University of Groningen Genetics of manta and devil rays ...Chapter 1 10 Figure 2: Bayesian...

University of Groningen

Genetics of manta and devil raysPoortvliet, Marloes

IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.

Document VersionPublisher's PDF, also known as Version of record

Publication date:2015

Link to publication in University of Groningen/UMCG research database

Citation for published version (APA):Poortvliet, M. (2015). Genetics of manta and devil rays: Evolution, population genetics and conservation ofa group of vulnerable pelagic filter-feeders. [Groningen]: University of Groningen.

CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).

Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.

Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.

Download date: 26-06-2020

https://www.rug.nl/research/portal/en/publications/genetics-of-manta-and-devil-rays(32cfb0c5-3652-4867-9c59-f7b9bcf60743).html



1General Introduction

Marloes Poortvliet

Chapter 1

8

Manta and devil rays of the Family Mobulidae (Order Myliobatiformes), collectively known as mobulids, comprise a group of 11 filter-feeding rays. They roam the pelagic habitat, as well as the continental margins of all the world’s oceans; they are also among the most captivating and charismatic of marine species. Similar to other elasmobranchs, mobulids share a vulnerable life history, characterized by slow growth and extremely low fecundity; yet they are subjected to intense and increasing fishing pressure across their entire range. As a consequence, eight out of 11 mobulids are classified on the International Union for the Conservation of Nature (IUCN) Red List as ‘Threatened’, ‘Vulnerable’ or ‘Near Threatened’, with the remaining three species listed as ‘Data Deficient’. Unfortunately, and despite their threatened status, management policies on the capture of mobulids are limited. This lack of protection is partly due to an absence of information on many aspects of mobulid life history, which complicates the development of management strategies beyond ‘general protection’. This PhD project was initiated to investi-gate the evolution and population genetics of this vulnerable group of elasmobranchs in order to assist in the development of scientific management guidelines

The general questions of interest were:

1. What are the evolutionary relationships within the Family Mobulidae, and what is the geological timing and pattern of their radiation? What were the probable mechanisms and drivers of mobulid speciation?

2. What is the spatial scale and connectivity among genetically defined populations of the spinetail devil ray, Mobula japanica? What have been the influences of past climate change on its historical population structure and demography?

3. Is there evidence for sex-biased dispersal in M. japanica?

4. What are the main anthropogenic threats to mobulids? How can this group of species be better protected?

1

Chondrichthyans

Chondrichthyans (cartilaginous fishes) are a group of jawed vertebrates that includes sharks, skates, rays and chimearas. Together with osteichthyans (bony fishes including tetra-pods), they represent one of two primary groups of jawed vertebrates, with fossils dating back ~420 My (Benton & Asher 2009). Chondrichthyans are divided into two major groups, the Ho-locephali (chimaeras) and Elasmobranchii (elasmobranchs). Elasmobranchii are in turn divided into Batoidae (skates and rays) and Selachii (sharks) (Figure 1), with batoids deviating from the ancestral shark-like body plan, and encompassing such diverse groups as guitarfishes, electrici-ty-generating torpedo rays, sawfishes and stingrays (Figure 2).

Although Chondrichthyans represent only a fraction of the extant biodiversity of jawed vertebrates, they exhibit an impressive range of life history strategies and morphological varia-tion. They fertilize via copulation, and embryos may be reared either internally with a placenta (viviparity), internally without a placenta (ovo-viviparity), or externally (true oviparity). Each reproductive strategy is distributed patchily throughout the chondrichthyan phylogeny, and has been lost and regained multiple times during chondrichthyan evolution (Compagno 2005).

Chondrichthyans are less productive and inherently more vulnerable to extinction than bony fishes (Myers & Worm 2005; Stevens 2000). Unlike bony fishes, which generally spawn millions of small eggs into the water column for external fertilization, chondrichthyans have ex-tremely low fecundity (Dulvy et al. 2014a), producing only a few hundred eggs during their lives. Anywhere from a few dozen to a single offspring are typically produced in one year.

Mobulids

Manta and devil rays of the Family Mobulidae (Superorder: Batoidea; Order: Myliobatidae) display dorso-ventrally flattened bodies with broad, well-developed pectoral fins and a whip-like tail. They are the largest extant group of rays inhabiting tropical, subtropical and warm temper-ate waters worldwide (Compagno & Last 1999a; Last & Stevens 1994). Mobulids are a unique group of rays, being the only batoids that developed the filter-feeding strategy (most others are benthic, and feed on crustaceans, mollusks, polychaetes and fishes). They are characterized by loss of dental function related to feeding (Adnet et al. 2012), the presence of cephalic lobes that direct prey into the mouth, and by a set of pre-branchial filter plates which are used to strain food particles from the water (Bigelow & Schroeder 1953; Coles 1916; Cortés et al. 2008). Their closest living relatives are the durophagous (shell-crushing) cownose rays (Family Rhinobatis), from which mobulids diverged around 34 Mya, based on the first occurrence of teeth without strain-marks caused by biomechanical stress due to grinding-type feeding (Adnet et al. 2012). Within the chondrichthyans, only three other species of cartilaginous planktivores exist, namely whale shark (Rhincodon typus), basking shark (Cetorhinus maximus) and the elusive megamouth shark (Megachasma pelagios); all three belong to the Selachii. Like other filter-feeders, mobulid distributions largely overlap with areas of high upwelling-related productivity and seasonal mi-gration patterns reflect temporal increases in upwelling (Anderson et al. 2011; Croll et al. 2012; Graham et al. 2012).

The 11 recognized mobulids are currently divided into two genera: (Mobula, Rafinesque 1810, and Manta, Bancroft 1829). Manta is comprised of two species, the oceanic manta, Manta birostris and the reef manta, Manta alfredi. Mobula contains nine species: Mobula japanica, Mobula mobular, Mobula tarapacana, Mobula thurstoni, Mobula kuhlii, Mobula eregoodootenkee, Mobula hypostoma, Mobula rochebrunei, and Mobula munkiana. Manta birostris, M. alfredi, M. mobular, M. japanica and M. tarapacana are among the larger rays in the Family, with Maximum Disc Widths (DWmax) of 700, 500, 520, 370 and 310 cm respectively.

9

General Introduction

1

Chapter 1

10

Figure 2: Bayesian phylogeny of all major Batoidea groups and three outgroup species (Holocephalii, Squa-lomorphii and Galeomorphii), based on 9000 nucleotides of the mitochondrial genome including nuclear genes RAG1 and SCFD2 (from Aschliman 2014). Black arrow indicates the phylogenetic position of the Order Myliobatoidae (stingrays), which contains the Family Mobulidae.

!

!10!

(Figure!1:!Maximum!Likelihood!phylogenetic!tree!of!25!vertebrate!species!representing!the!main!Chondrichthyes!lineages,!based!on!9409!nucleotides!of!the!mitochondrial!genome!(from!Inoue!et!al.,!2010).! !!!

!!Figure!2:!Bayesian!phylogeny!of!all!major!Batoidea!groups!and!three!outgroup!species!(Holocephalii,!Squalomorphii!and!Galeomorphii),!based!on!9000!nucleotides!of!the!mitochondrial!genome!including!nuclear!genes!RAG1!and!SCFD2!(from!Aschliman!2014).!Black!arrow!indicates!the!phylogenetic!position!of!the!Order!Myliobatoidae!(stingrays),!which!contains!the!Family!Mobulidae.!!!

!

!10!

(Figure!1:!Maximum!Likelihood!phylogenetic!tree!of!25!vertebrate!species!representing!the!main!Chondrichthyes!lineages,!based!on!9409!nucleotides!of!the!mitochondrial!genome!(from!Inoue!et!al.,!2010).! !!!

!!Figure!2:!Bayesian!phylogeny!of!all!major!Batoidea!groups!and!three!outgroup!species!(Holocephalii,!Squalomorphii!and!Galeomorphii),!based!on!9000!nucleotides!of!the!mitochondrial!genome!including!nuclear!genes!RAG1!and!SCFD2!(from!Aschliman!2014).!Black!arrow!indicates!the!phylogenetic!position!of!the!Order!Myliobatoidae!(stingrays),!which!contains!the!Family!Mobulidae.!!!

Figure 1: Maximum Likelihood phylogenetic tree of 25 vertebrate species representing the main Chondrichthyes lineages, based on 9409 nucleotides of the mitochondrial genome (from Inoue et al., 2010).

1

11

The remaining Mobula species are smaller, with a DWmax of up to 180 cm (Couturier et al. 2012). Morphologically, Manta is distinct from Mobula in exhibiting a terminal mouth, while Mobula species share a ventral placement of the mouth. The structure of mobulid teeth and filter plates has been extensively studied. Adnet et al. (2012) divided mobulids into 3 main groups based on the morphology of teeth, while Paig-Tran et al. (2013) broadly divided 9 of the 11 mobulids into three different groups, based on the presence of denticles and or cilia/secondary structure on the surface of filter plates (Figure 3 and Table 1).

Mobula japanica

M. japanica is mainly pelagic and is found inshore as well as in oceanic environments. It is believed to have a circumglobal distribution throughout all sub-tropical and tropical oceans. It has been suggested that M. japanica is conspecific to M. mobular, a species that only occurs in the Mediterranean Sea and possibly the adjacent Eastern Atlantic Ocean. The two species are morphologically highly similar, with only minor differences in DWmax (M. mobular DWmax= 550 cm), body proportions (M. mobular reaches a larger DWmax relative to the rest of its body), and tooth morphology (Adnet et al., 2012; Notarbartolo di Sciara, 1987).

M. japanica is one of the more common mobulids in the Southern Sea of Cortez, Mexico, where its seasonal and geographical movement patterns have been studied based on both fisheries catch and tagging data. Catch records from artisanal fishermen collected over a period of 4 years (1982-86) showed that M. japanica moves in small aggregations even though it is not considered to be a true shoaling species. Catches progressively increased from March to July each year, whereas during the winter only very few M. japanica remained (Notarbartolo di Sciara 1988). The seasonal increase in abundance also matched offshore to inshore movements of aggregations from deeper to shallower waters, often in unison with seasonal increases in local prey density. This pattern was confirmed by Croll et al. 2012 based on satellite tagging data of 10 M. japanica individuals. These authors showed that seasonal migration patterns matched temporal increases in upwelling and tracked seasonal patterns in euphausiid (zooplankton) abundance (de Silva-Davila & Palomares-Garcia 1998; Gomez-Gutierrez et al. 2010) (Figure 4).

Information about reproductive behavior in M. japanica is limited. Owing to the presence of reproductively active males during autumn, the southern Gulf of California is believed to serve as an important spring and summer mating ground (Notarbartolo di Sciara 1988). Howev-er, although one female showed evidence of recently having given birth, no juvenile M. japanica have ever been observed in this region. Hence, it is unknown if females give birth in the Gulf of California or if they move to other (offshore) locations for pupping. Additionally, no information is available on possible philopatry to specific breeding or pupping sites—a common behavioral pattern for many chondrichthyan species (Hueter et al. 2004).

Other mobulid species

For the remaining Mobula rays, information about distribution, feeding range and breeding behavior is extremely limited.

Mobula taracapana is probably circumglobal in subtropical and tropical waters but, at present, it is known from only a few scattered locations across the Indian, Pacific and Atlantic Oceans. This large pelagic mobulid with a DWmax of around 370 cm occurs primarily in oceanic regions, but is occasionally found in coastal waters (Notarbartolo di Sciara 1988). Recent tagging data from the central North Atlantic Ocean showed that this species moves across thousands of kilometers from the tagging location in the Azores Islands and (amazingly) descends to depths of almost 2000 m, where it is thought to forage in the deep scattering layer (Thorrold et al. 2014). It

1


Chapter 1

12

Fgure 3: Characteristic features of Manta and Mobula rays. A) Terminal placement of the mouth in Manta; B) ventral placement of the mouth in Mobula; C) filter plate of Manta; D) close-up of filter lobes in Manta; E) fil-ter plate of Mobula; F) close-up of filter lobes in Mobula; G) dorsal view of teeth in Manta sp. with close-up of peg-like teeth; H) cobblestone toothplate in Mobula tarapacana; I) peg-like teeth in Mobula japanica; J) comb-like teeth (subgroup I) in Mobula thurstoni; K) comb-like teeth (sugroup II) in Mobula rochebrunei. Lingual (li.) or occlusal (o.) view indicated on the right hand side of each tooth.

Opposite page, Table 1: Information about the 11 mobulid species, with genus and species name, taxonomic reference, geographic distribution, habitat, DWmax, placement of the mouth, tooth morphology group (Adnet et al. 2012), the presence (+) or absence (-) of denticles (dent.), cilia, secondary structure (SS) or smooth sur-face epithelium on filter plates, filter plate group (based on Paig-Tran et al. 2013), and IUCN RedList status. VU: vulnerable; NT: Near Threatened; EN: Endangered; DD: Data Deficient.

1

13

1

!

!

13#

Species'n

ame'

!!!!!C

ommon

!nam

e!!

Tax.!re

f.!Distrib

ution!

Occuren

ce!

Dwma

x!(cm

)!Placem

ent!!

mou

th!

Teeth!grou

p!Ca

udal!

spine?

!Filte

r!plates!

!!IUCN

!Status

!

####

####

####

###

Dent.#

Cilia#

SS#

SmE#

Group#

##

Man

ta%biro

stris%

#####G

iant#m

anta#ra

y#Walba

um,#1

792#

Circum

glob

al#in

#trop

ical#

and#su

btropical#w

aters#

Oce

anic#and

#co

astal#

700#

Term

inal#

PegElik

e#teeth#

Yes#

+#E#

+#E#

1#VU

#

Man

ta%alfredi%

%%%%%R

eef#m

anta#ra

y#Krefft,#186

8#Indian

#and

#Pacific#Oce

an,##

in#tr

opical#w

aters #

ReefE

asso

ciated

#50

0#Te

rminal#

?#No#

?#?#

?#?#

?#VU

#

Mob

ula%tarapa

cana

%%%%%%C

hilean

#dev

il#ray#

Philipp

i,#18

92#

Circum

glob

al#in

#trop

ical#

and#su

btropical#w

aters#

Oce

anic#and

#co

astal#

370#

Ventral#

Cobb

leston

e#tooth#plates#

No#

+#+#

E#E#

1#DD

#

Mob

ula%japa

nica%

%%%%%S

pine

tail#de

vil#ray

#Müller#a

nd#

Henle,#184

1#Circum

glob

al#in

#trop

ical#

and#su

btropical#w

aters#

Oce

anic#and

#co

astal#

310#

Ventral#

PegElik

e#teeth#

Yes#

E#E#

E#+#

4#NT#

Mob

ula%mob

ular%

%%%%%G

iant#dev

il#ray#

Bonn

aterre,#

1788

#Med

iterran

ean#Se

a#Oce

anic#and

#co

astal#

520#

Ventral#

PegElik

e#teeth#

Yes#

?#?#

?#?#

?#EN

#

Mob

ula%thurston

i%%%%%%S

moo

thtail#de

vil#ray

#Lloy

d,#190

8#Circum

glob

al#in

#trop

ical#

and#su

btropical#w

aters #

Oce

anic#and

#co

astal #

180#

Ventral#

CombElik

e#teeth#

subg

r.#1 #

No#

+#E#

E#+#

2#NT#

Mob

ula%eregoo

dootenkee%

%%%%%P

ygmy#de

vil#ray

#Blee

ker,#18

59#

Indo

EW#Pacific#region

,#trop

ical#w

aters#

Coastal#

100#

Ventral#

CombElik

e#teeth#

subg

r.#1#

No#

E#E#

E#+#

4#NT#

Mob

ula%kuhlii%

%%%%%S

hortfin

#dev

il#ray#

Müller#a

nd#

Henle,#184

1#Indo

EW#Pacific#region

,#trop

ical#w

aters#

Coastal#

100#

Ventral#

CombElik

e#teeth#

subg

r.#1#

No#

E#+#

E#E#

3#DD

#

Mob

ula%mun

kian

a%%%%%%M

unk’s#d

evil#ray#

Notarba

rtolo#di#

Sciara,#1

987 #

East#Pacific#Oce

an,#

trop

ical#and

#s ubtropical#

waters#

Coastal#

110#

Ventral#

CombElik

e#teeth#

subg

r.#2 #

No#

+#E#

+#E#

1#NT#

Mob

ula%rochbrun

ei%

%%%%%Lesser#G

uine

an#dev

il#ray#

Vaillan

t,#18

79#

East#Atla

ntic#Oce

an,#

trop

ical#w

aters#

Coastal#

130#

Ventral#

CombElik

e#teeth#

subg

r.#2#

No#

?#?#

?#?#

?#VU

#

Mob

ula%hypo

stom

a%%%%%%A

tlantic#dev

il#ray#

Banc

roft,#1

831#

West#A

tlantic#Oce

an,#

trop

ical#w

aters #

Coastal#

120#

Ventral#

CombElik

e#teeth#

subg

r.#2 #

No#

+#E#

E#+#

2#DD

#


Chapter 1

14

has been suggested that M. taracapana may be a more generalist feeder than other Mobulidae, or even possibly ichthyophagous (Notarbartolo di Sciara 1988).

Mobula thurstoni is probably circumglobal in all subtropical and tropical oceans, but this has not been confirmed. Tagging data indicate that individuals can travel across thousands of kilometers in several months (Croll, unpublished data). This ray reaches a DWmax of 180 cm and is mainly found in shallow, neritic waters (<100 m) (reviewed by Couturier et al. 2012).

Mobula munkiana is a recently described inshore species endemic to the Eastern Pacific (from the Baja Peninsula, Mexico to Peru) and is particularly common in the Sea of Cortez. The species reaches a DWmax of ~110 cm and occurs mainly inshore over the continental shelf.

M. munkiana is the only mobulid that is consistently observed in shoals. It is not known whether shoaling is seasonal or a permanent behavioral feature. The presence of shoals is often detected by simultaneously jumping individuals. Size (but not sexual) segregation has been ob-served in the Sea of Cortez. Pupping has been observed in Bahía de La Paz during May and June (Notarbartolo di Sciara 1988).

Mobula eregoodootenkee reaches a DWmax of 100 cm and is locally common within its wide tropical Indo-Pacific and Northern Indian Ocean distribution. It is not known to enter the epipe-lagic zone and only dwells close to shore over the continental shelf. Mating and pupping occur in shallow water and juveniles remain in these areas (Notarbartolo di Sciara 1987).

Mobula kuhlii, Mobula hypostoma and Mobula rochebrunei occur in the Indo-Pacific re-gion, the Western Atlantic and Eastern Atlantic respectively. Almost nothing is known beyond a taxonomic record (Notarbartolo di Sciara 1987).

Manta birostris (giant manta ray) is the largest of all mobulids, with a DWmax of ~700 cm. It is a true pelagic species and widely distributed in all tropical and subtropical oceanic waters, as well as in coastal areas over continental shelves, near seamounts, and in upwelling zones (Mar-

Fgure 4: Weighted fixed-kernel density distribution (blue: 95 %; red: 50 %) of 13 tagged Mobula japanica individuals, June-September (From Croll et al. 2012).

1

15

shall et al. 2009). Rare or seasonal sightings of M. birostris at locations in New Zealand (Duffy & Abbott 2003), southern Brazil (Luiz et al. 2009), Uruguay (Millessi & Oddone 2003), the Azores Islands, and the eastern coast of the USA (Bigelow and Schroeder 1953), suggest that this spe-cies makes significant seasonal migrations. Tagging data from six smaller M. birostris individuals (DW <450 cm) around the Yucatan peninsula (Mexico) detected limited foraging movements (~100 km) over a period of one month, associated with broad thermal fronts near an upwelling zone (Graham et al. 2012).

Manta alfredi (reef manta ray) was only recently re-described. It is smaller than the giant manta ray with a DWmax of ~500 cm. It occurs near coral and rocky reefs, as well as along coastlines with consistent upwelling. It is patchily distributed in the Indian and Pacific Oceans (Marshall et al. 2009). Long-term sighting records of M. alfredi at established aggregation sites suggest that this species is more resident to tropical waters and may exhibit small home ranges and short seasonal migrations (Marshall & Bennett 2010).

Taxonomic issues

Despite their iconic status, the systematics of mobulids is cluttered with competing taxo-nomic circumscriptions (mainly based on morphology and tooth anatomy) and poor resolution of currently available phylogenies, i.e., the paraphyletic recognition of Manta and Mobula, in which Manta species are nested within Mobula species (reviewed by Aschliman 2014). Addi-tionally, for several species it is still not clear whether they comprise distinct lineages or are merely geographically separated morphological variants of the same species (Marshall et al. 2009; Notarbartolo di Sciara 1987).

Life history vulnerabilities and fisheries

All mobulid species display life history traits that make them vulnerable to overexploita-tion (Dulvy et al., 2008; Garcia et al., 2008; Dulvy et al., 2014). These include ovo-viviparous or matrotrophic reproduction (nourishment of embryos derived from the mother without the presence of a placenta), large size at birth, slow growth, high maximum age, delayed age of first reproduction, and extremely low fecundity (reviewed by Couturier et al., 2012; Cuevas-Zimbrón et al., 2012). Even by chondrichthyan standards, mobulid fecundity is low (Dulvy et al. 2014b). A recent estimate of manta ray maximum intrinsic population growth rate, rmax (a proxy for extinction risk based on individual growth rate, annual pup production and age at maturity) showed that rmax is one of the lowest known of the 106 shark and ray species for which compa-rable demographic information is available (Figure 5). Population growth rate (rmax) has not been estimated for Mobula, but likely is similarly low to Manta.

The vulnerable life history of mobulids is especially problematic in light of high and increasing anthropogenic pressures. Mobulids are increasingly being targeted in artisanal fish-eries across Asia, motivated by the use of their filter plates in Chinese medicine. Additionally, the annual bycatch mortality of mobulids in global tuna purse-seine-fisheries is thought to be substantial. As a consequence of high catch rates, local mobulid populations are declining. In reaction to this pressure, the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species (an international standard for species extinction risk) has evaluated eight of 11 mobulid species. M. mobular is listed as ‘Endangered’, M. birostris, M. alfredi and M. rochebrunei are listed as ‘Vulnerable’, and M. japanica, M. thurstoni, M. munkiana and M. ere-goodootenkee as ‘Near Threatened’. The remaining three species are listed as ‘Data Deficient’.

Heavy fishing pressure can lead to dangerously small populations and eventual disruption of behavior and mating, which can heighten extinction risk through the ultimate loss of genetic

1


Chapter 1

16

variation. Loss of variation may also affect a species’ ability to adapt to changing environmental conditions (Barrett & Schluter 2008; Keller & Waller 2002) and therefore also presents increased extinction risk. Although genetic metrics are not directly used in IUCN species assessments (Rivers et al. 2014), the organization has acknowledged the need to prevent loss of genetic biodiversity within a species (or stock); preventing the loss of genetic variation is also a specific goal of the Convention of Biological Diversity (Laikre 2010). Population genetic studies provide quantitative data for evaluating population structure, effective population size, loss of diversity, and estimates of connectivity (Avise 2008).

Population structure and connectivity

Commonly asked questions in fundamental biology and marine conservation of mobile species are: how many populations (also called stocks in fisheries) of a given species are there, how large are they, how do they move around and how do they interact? Populations are identified by both their discreteness, as well as connectedness throughout their biogeographic range (Waples & Gaggiotti 2006). Defining a population a priori, for example based on a geo-graphic region is seldom useful and may lead to discrepancies between biological populations and management populations. For example, the population may move seasonally between fixed management areas or separate fish populations may occur in a single management area (Bowen et al. 2005). A mismatch may lead to mismanagement leading to loss of genetic diversity and subsequent decline of the population; alternatively, it may lead to an inflated allocation of con-servation resources (Waples 1998)

Many definitions of a population can be found in the literature but in general the term refers to a group of organisms whose trajectory is largely independent from other such groups (Carvalho & Hauser 1994). Two major types of biological definitions can be identified: those reflecting an ecological/demographic paradigm and those reflecting an evolutionary/genetic paradigm. A general working definition of ‘population’ for the ecological paradigm is ‘a group of individuals of the same species that co-occur in space and time and have an opportunity to

Fgure 5: Maximum intrinsic rate of population increase for manta rays as compared with 106 other chondrich-thyans. Values of rmax (x-axis) and frequency of chondrichthyan species (y-axis). (From Dulvy et al. 2014b).

1

17

interact with each other demographically (e.g. competition, social and behavioral interactions, including mating). For the evolutionary paradigm a population genetic view is more useful. Here the focus is genetic cohesiveness through reproductive interactions within the population unit rather than between population units (Waples & Gaggiotti 2006). In practice, population structure encompasses all of these components: complex interactions among the life history characteristics (i.e. larval stages, homing behavior), demographic parameters (i.e. reproduc-tion, recruitment, growth and mortality) and genetic processes (i.e. drift, gene flow, selection, mutation). Disentangling these many processes is not easy, but has been greatly facilitated by a strong theoretical basis in combination with the development of highly polymorphic genetic markers and more powerful sequencing and analysis methods (Avise 2010; Curole & Kocher 1999). Hence, the assessment of genetic structure is increasingly robust and (most importantly) informative and practical.

Populations of many marine species encompass an extensive range of spatial scales—from single bays to ocean-basin-wide (Ward et al. 1994). Superior swimming ability, absence of barriers, currents and the semi-continuous nature of most of the world’s oceans all facilitate long-range dispersal and thereby the potential to maintain large-scale populations (Palumbi 1994; Waples 1987). Until about 25 years ago, it was widely believed that there was little or no population structure of species in the sea for exactly these reasons. It is now known, howev-er, that despite the vastness of the oceans and the long-range dispersal capabilities of many marine vertebrates, considerable population structure does exist (reviewed by Ward et al. 1994). Palumbi (1994) reviewed ways in which populations with high dispersal potential could develop genetic subdivision: i) limits to gene flow from barriers created by oceanic circulation patterns, currents, and tectonic plate boundaries; ii) isolation-by-distance; iii) behavioral control of dispersal by migration; iv) natural selection due to environmental gradients; and v) historical subdivision of populations (vicariance) due to paeloclimatic changes associated with the ice ages and sea level that caused local extinction followed by recolonization.

Ward et al. 1994 reviewed population genetic data for marine fishes (all habitat types) and found that the mean FST (a measure of total genetic diversity that is allocated among popula-tions) was 0.062 (N=57 studies) as compared to 0.108 for anandromous fishes (i.e., salmon) (N=7 studies), and 0.222 for freshwater fishes (N=49 studies). When the marine fishes were further partitioned by habitat types, results were even more striking. FST values in the two shark species were extremely low (FST=0.0094 and 0.0076, both sampled from nine locations in Northern Australia), whereas FST values for reef-associated teleost species varied around the average found in the aggregated habitats. Regional differences were also found (e.g., Doherty et al. 1995; Planes et al. 2001) and depend to some extent on the pelagic larval duration of the species (Bernardi et al. 2001; Crandall et al. 2008).

Review of population genetic studies in chondrichthyans

Chondrichthyan population genetics has become an increasingly popular topic of study over the last decade, uncovering genetic structure across a wide range of geographical dis-tances (Supplementary Table S1). Within the Carcharhiniformes (ground sharks), species have been found that have structured populations between nearby estuaries, while others show no structure whatsoever across vast expanses of ocean. Within the Lamniformes (mackerel sharks), which mostly consists of large, oceanic species, structured populations exist between ocean basins, but usually not within. For example, the basking shark (Cetorhinus maximus) and the shortfin mako (Isurus oxyrinchus) both show genetic structure between the Atlantic Ocean and Indian-Pacific Oceans, but no structure within these regions (Hoelzel et al. 2006; Schrey & Heist 2003). Myliobatidae (stingrays), Pristiformes (sawfishes), Rajiformes (skates) and Squaliformes

1


Chapter 1

18

1

(dogfish sharks) generally show some structure across short geographic distances—or even the presence of closely related sister-species. For example, white-spotted eagle rays were shown to consist of several reciprocally monophyletic, cryptic lineages in the Indian and Pacific Oceans (Aetobatus narinari; Richards et al. 2009).

So is there a common pattern, which can help us predict the scale of population genetic structure in chondrichthyans? First of all, rather than being influenced by oceanic circulation patterns that enhance or restrict dispersal of teleost larvae, chondrichthyan dispersal is mostly dependent on active dispersal of adults. Dispersal varies widely. Vast expanses of deep water may represent barriers for coastal species that rely on short distances between habitat patches, resulting in genetic structure over small distances (e.g., blue-spotted maskray, Neotrygon kuhlii: Arlyza et al. 2013; shovelnose guitarfish, Rhinobatos productus: Sandoval-Castillo et al. 2004; spot-tail shark, Carcharhinus sorrah: Ovenden et al. 2009). See Supplementary Table S1 for details. In contrast, highly vagile oceanic species may show population homogeneity at the scale of ocean basins (e.g., whale shark, Rhincodon typus: Vignaud et al. 2014; blue shark, Prionace glauka: Ovenden et al. 2009; shortfin mako, Isurus oxyrinchus: Schrey & Heist 2003; basking shark, Cetorhinus maximus: Hoelzel et al. 2006). See Supplementary Table S1 for details.

Second, reproductive behavior can play an important role in the geographic scale of genet-ic structure (Bowen et al. 2005). Many sharks and rays display philopatry, with females repeat-edly returning to their natal site for breeding and pupping, whereas males roam more widely (Hueter et al. 2004). This behavior is thought to explain strong population structure across short geographical distances, even in highly vagile (oceanic) species (Supplementary Table S1). The white shark is probably the most extreme example. It has been shown to undertake trans-oce-anic migrations across thousands of kilometers, yet females annually return to specific breeding areas resulting in strong genetic structure both between and within ocean basins (Pardini et al. 2001). Philopatry is also though to explain genetic structure in other highly vagile species such as blacktip sharks (Carcharhinus limbatus: Keeney & Heist 2006), and hammerhead sharks (Sphyrna lewini: Daly-Engel et al. 2012).

And third, it has also become clear that genetic structure of some chondrichthyan popu-lations is not only influenced by life history traits but also by past vicariant events such as the closing of the Isthmus of Panama and Pleistocene glacial-interglacial cycling (Supplementary Table S1). For example, in many species with warm-water distributions, population genetic structure between ocean basins has been attributed to the rise of the Isthmus of Panama (~3.5 Mya), which closed the connection between the East Pacific and Atlantic Oceans. The frigid waters around the Cape of Good Hope has also been a barrier, with only intermittent dispersal between the Atlantic and Indian Oceans during periods of increased Agulhas leakage (Peeters et al. 2004). Both whale sharks and white sharks show divergent mitochondrial lineages in the Atlantic and Indian/Pacific Ocean, which are thought to result from vicariant isolation across this barrier (Gubili et al. 2011; Vignaud et al. 2014). The Sunda/Sahul shelf north of Australia, which was exposed as recently as the Last Glacial Maximum (LGM) 18000 y ago, severed the connection between the Indian and Pacific Ocean populations of species such as the pig-eye shark (Carcharhinus amboinensis: Tillett et al. 2011) and the white-tip reef shark (Triaenodon obesus: Whitney et al. 2012). And on smaller spatial scales, the northern Atlantic part of the range of the thornback ray (Raja clavata) was pushed southwards during the LGM, but was then recolonized from the south when ice started to move away, with currently limited connectivity between regions (Chevolot et al. 2006).

Taking into consideration the three factors above, we hypothesized that M. japanica would likely show genetic structure across intermediate geographic scales, both between ocean basins as well as within. The species is not restricted to a coastal habitat, but based on tagging data only has an intermediate capacity for dispersal, with distances of 1000-1500 km covered within

19

several months. No ocean-basin scale migrations were observed, as in other pelagic chondrich-thyans, like whale sharks and basking sharks (Eckert et al. 2002; Gore et al. 2008). There is no information on the existence of philopatry in M. japanica. However, fisheries catch and tagging data indicate an annual seasonal migration pattern (Notarbartolo di Sciara 1988), which in turn is suggestive of site fidelity, either for breeding or feeding. If site fidelity indeed exists, this would likely also result in restricted connectivity between more remote regions. Whether vicari-ance has played a role was unknown at the outset of this study but hypothesized as a possible structuring influence for M. japanica.

Technical issues

Sampling

In highly migratory species, the resolution of populations can be confounded by several factors. High levels of gene flow result in low levels of genetic differentiation, and sampling a specific geographical area under the assumption that it represents a population may simply be incorrect (Waples & Gaggiotti 2006). This is because demographically independent populations may mingle in common feeding grounds, during migratory phases or when gene flow is sex-bi-ased (Bowen et al. 2005). This makes sampling strategies challenging. The use of genetic mark-ers with different modes of inheritance, as well as surveys of distinct life states and especially breeding populations, are therefore of paramount importance when resolving the spatial extent of population structure. Further strategies to minimize sampling errors include: 1) collection of fixed size classes in an effort to minimize overlapping generations in a sampled location; 2) sampling far enough apart; and 3) the inclusion of temporal sampling of the same site, so that effects can be compared over generations (Waples 1998).

For M. japanica, a general lack of information about migratory patterns and reproductive behavior made it impossible to design a foolproof a priori sampling regime for intra-specific studies. Moreover, because the species occurs in oceanic environments and can be highly elusive, samples are not easily obtainable even when good, potential sampling locations are known. This meant that sampling could only be conducted on an opportunistic basis in coop-eration with tuna purse seine fisheries, artisanal fisheries and some targeted catches. For the present study a total of 263 samples was collected from eight locations in the Atlantic, Indian and Pacific Oceans. At least nine individuals were collected per location and in most cases many more.

For interspecific relationships among mobulids, sampling is of no less importance. Taxon sampling based on an exemplar approach to infer higher-level evolutionary relationships can also be a source of phylogenetic error (Hillis et al. 2003; Pollock et al. 2002). Ideally, individuals of each species need to be sampled from locations across its entire geographic range. In the present study, samples were collected in a similar manner, from bycatch and targeted fisheries, and in a few cases from natural history museum collections.

Genetic markers

Microsatellites. Microsatellites are tandem repeat motifs of two to five bases, scattered throughout the genomes of eukaryotes. They are co-dominant, assumed to be neutral, and are often highly polymorphic, making this class of markers a popular choice for addressing popula-tion genetic questions (Ellegren 2000; Jarne & Lagoda 1996). Length polymorphism in microsat-ellites is thought to arise mainly by slippage mechanisms or recombination following a stepwise mutation model, where the size of the new allele depends on the size of the allele that mutated

1


Chapter 1

20

1

(Li et al. 2002). Because of their fast mutation rate, which is estimated to be between 10-3 and 10-5 per generation (Sun et al. 2012; Weber & Wong 1993), even closely related populations can show marked differences in repeat lengths. Although the assumption of neutrality is generally valid, exceptions are known but can usually be detected in the data set and removed as neces-sary. Other technical issues common to microsatellites such as null alleles (i.e. non-amplification of some alleles), stutter (Taq polymerase slippage during PCR amplification) and large allele drop-out (higher amplification rates of shorter alleles) (O’Connell & Wright 1997) can also be corrected for. The main critique of this class of marker is the lack of a reliable mutation model (Sainudiin et al. 2004). Forward and back mutation under the stepwise model creates homo-plasy, which can interfere with some estimates. Despite these issues, microsatellites remain a powerful category of markers in the field of population genetics.

mtDNA. Mitochondrial DNA is effectively a single locus with haploid and maternal inher-itance, resulting in a four-fold lower effective population size than nuclear markers (Birky et al. 1989). Because of its reduced effective population size, mtDNA provides higher resolving power than nuclear DNA in cases where populations have not reached migration/drift equilib-rium. Additional advantages are: 1) mtDNA reflects the female lineage only and, therefore can provide information unobtainable by a nuclear marker (this is particularly important in groups such as chondrichthyans, where there is evidence for reproductive philopatry in females, but not males); 2) it allows inferences of historical demography (Avise et al. 1988); and 3) its fast evolutionary rate provides the chance of recovering the pattern and tempo of recent historical events without extensive sequencing effort.

Despite these advantages, however, mtDNA can also be uninformative in some species if only one or a few genes are used (Galtier et al. 2009). This is especially the case when the rate of evolution is slow, as in chondrichthyans in general (Martin et al. 1992). The only way to compensate for this slow rate is to increase the length of sequence data (Alexander et al. 2013; Morin et al. 2010; Shamblin et al. 2012). For example, based on 93 complete mtDNA genomes (mitogenomes), Feutry et al. (2014) were able to discriminate among single river drainages as discrete management units for the conservation of the speartooth shark (Glyphis glyphis). Using the full mitogenome, they were able to illustrate that the often used Control Region and Cytochrome Oxidase I gene are not necessarily informative (i.e., the situation is clear if these se-quences show distinct haplotypes; but if not, the absence of distinct haplotypes is not evidence of absence of structure).

Next Generation Sequencing

The advent of next-generation sequencing (NGS) makes it easier and cheaper to obtain large mitogenome data sets, in comparison with traditional Sanger sequencing using long PCR methods. The application of NGS seems almost endless, allowing for rapid advances in many fields related to biological sciences, including intra-specific studies. Whereas whole mitoge-nome sequencing was previously mostly used in inter-specific phylogenetic studies, mitoge-nomes are now increasingly being used to resolve population genetic structure within species (for example, each of the three ‘ecotypes’ within the cosmopolitan killer whale was shown to consist of a strongly supported clade with divergence times ranging from ~150-700 Kya (Morin et al. 2010).

NGS platforms perform massively parallel sequencing, and generate millions of fragments of DNA from a single sample. Generally, the methodology involves template preparation, library preparation, library amplification, sequencing and imaging, and data analysis (Figure 6). Tem-plate preparation involves building a library of nucleic acids (DNA or cDNA) by fragmentation

21

(shearing of the DNA or cDNA into smaller pieces) and the ligation of adapters (oligonucleotides with a known sequence) to the 5’ and 3’ ends. Library fragments are then clonally amplified and sequenced. Once sequencing is complete, adapter and low-quality sequences are removed, and the data is assembled either using a reference genome, or a de novo alignment. Analysis of the sequences can include a wide variety of bioinformatic assessments, including genetic variant calling for detection of single nucleotide polymorphisms (SNPs) or the insertion or deletion of 1 or more bases (indels), detection of novel genes or regulatory elements, and assessment of transcript expression levels.

There are various NGS platforms, which mainly differ in how sequencing is performed. The two techniques are sequencing by synthesis and ligation-based sequencing (Table 2). Each platform has advantages and disadvantages (Grada & Weinbrecht 2013), and choosing a plat-form for a large part depends on the requirements of a particular project, as well as financial considerations. Read length and total yield per run are the key considerations in the choice of a particular instrument (Glenn 2011) (Table 2). For example, long reads (>500-1000 bp) are optimal for initial genome and transcriptome characterization, because longer pieces assemble more efficiently than shorter pieces. Alternatively, the lower costs and increased number of reads associated with shorter read-lengths (from 75-250 bp) are better suited for re-sequencing and for frequency-based applications.

1


Chapter 1

22

1

!

!22#

#######################

#Figure#6:#Next#Generation#Sequencing#workflow,#including#template#preparation,#fragmentation,#adapter#ligation,#library#amplification#(either#through#emulsion#PCR#or#cluster#generation),#sequencing#and#imaging,#and#data#analysis.

Figure 6: Next Generation Sequencing workflow, including template preparation, fragmentation, adapter ligation, library amplification (either through emulsion PCR or cluster generation), sequencing and imaging, and data analysis.

23

1

Table 2: Characteristics o

f the fo

ur most p

opular se

quencing platforms. Instrument, company, sequencing metho

d, amplificatio

n metho

d, th

e maximum

num

ber o

f bases per re

ad, the cost o

f reagents per ru

n, and

the percentage or e

rrors. Based on Glen (2011), w

ith upd

ated inform

ation available from

http://www.m

olecularecologist.com

/next-‐gen-‐fieldguide-‐2014/.

Instru

men

t Co

mpa

ny

Sequ

encing

metho

d Am

plifica

tion

metho

d M

illions

of r

eads

/run

M

ax.

base

s/re

ad

Reag

ent c

ost/ru

n Erro

r rate %

454 GS Jr. Titanium

Ro

che

Synthesis

(pyosequ

encing)

emPC

R 0.1

400

$1,000

1

454 FLX Titanium

Ro

che

Synthesis

(pyosequ

encing)

emPC

R 1

400

$6,200

1

454 FLX+

Roche

Synthesis

(pyosequ

encing)

emPC

R 1

650

$6,200

1

MiSeq

Illum

ina

Synthesis

Bridge PCR

15-‐22

600

$750-‐1500

0.1

NextSeq

Illum

ina

Synthesis

Bridge PCR

130-‐400

300

$1000-‐4000

0.1

HiSeq

Illum

ina

Synthesis

Bridge PCR

300-‐6000

250

$1000-‐15000

0.1

SOLiD

Life Techn

ologies

Ligatio

n em

PCR

1410

110

$10,500

<0.1

Ion Torrent P

GM

Life Techn

ologies

Synthesis (H

+ detectio

n)

emPC

R 314 chip: 0.475

400

$350-‐450

~1

316 chip: 2.5

400

$550-‐650

~1

318 chip: 4.75

400

$750-‐850

~1


Chapter 1

24

1

Outline of this thesis

To be able to address the questions posed in this thesis, obtaining good species and population-level sampling was of paramount importance. I therefore created an international network of collaborators, including observers on board tuna purse seine vessels, local research-ers and artisanal fishermen, which enabled me to accumulate an adequate number of samples from all ocean basins. I then used both NGS of mitogenomes, as well as traditional Sanger sequencing of nuclear and mitochondrial genes, and microsatellite genotyping to elucidate intra- and inter-specific relationships of mobulids.

In Chapter 2 and 3 I describe the development of molecular markers for this group of spe-cies. Chapter 2 deals with the development and testing of nuclear microsatellite loci for Mobula japanica, which were subsequently used to analyze the population genetic structure within this species. In Chapter 3 I sequenced the entire mitogenome of one M. japanica individual using cloning and Sanger sequencing techniques. This reference mitogenome sequence then served as a ‘backbone’ for the assembly of NGS-generated mitogenomes, which were used in both the phylogenography of M. japanica and the broader mobulid phylogeny.

Genetic studies within rare or difficult-to-sample groups of are often limited by the avail-ability of specimens. In such cases, museum collections form an easily accessible source of samples; however, the DNA obtained from such samples is often of low quality and unsuitable for many downstream applications. In Chapter 4 I explored the use and effectiveness of a “bait-based” method for enrichment of target sequences, in combination with NGS sequencing for use with degraded DNA samples.

In Chapter 5 I inferred the evolutionary relationships among the different mobulid species. I used NGS-generated mitogenomes, as well as an extended data set of two mitochondrial and two nuclear genes. Additionally, based on the estimated mutation rate, the mitogenome phy-logeny and two fossil calibration points, I estimated divergence times in mobulid evolution, and speculate about drivers and mechanisms of mobulid evolution.

In Chapter 6 I investigated the phylogeographic structure of one of the larger mobulid species, M. japanica, across its circumtropical distribution. For this, I used 60 NGS-generated mitogenomes from widely spaced geographic locations (Atlantic, Indian and Pacific Ocean ba-sins) in combination with a species-specific molecular clock (Chapter 5). Additionally, I investi-gated demographic changes in relation to historical climate change over the last 2.5 Mya. And finally, I used the 11 microsatellite loci (Chapter 2), two mitochondrial genes and a much larger set of samples to elucidate global population genetic structure, compare resolution with the mitogenome data on the smaller sample set, and to determine whether M. japanica displays sex-biased dispersal.

Chapter 7 reviews life history characteristics of mobulids, identifies global and local threats from targeted and bycatch mortality, and discusses mobulid conservation issues and solutions.

Finally, in Chapter 8 I synthesize the main insights developed from this thesis. I discuss the findings from Chapters 2 – 7, in relation to the existing literature.

25

1


1

Supp

lem

enta

ry m

ater

ial

Page

25

– 39

, Sup

plem

enta

ry T

able

S1:

List

of p

opul

atio

n ge

netic

stud

ies o

f cho

ndric

hthy

an sp

ecie

s. W

ith O

rder

, sci

entif

ic n

ame

and

com

mon

nam

e of

the

stud

ied

spec

ies;

the

dist

ribut

ion,

ha

bita

t and

vag

ility

of t

he st

udie

d sp

ecie

s; sa

mpl

ing

loca

tions

, gen

etic

mar

kers

use

d, re

sults

, and

the

refe

renc

e fo

r eac

h st

udy

O

rder

Sp

ecie

s nam

e Di

strib

utio

n H

abita

t Va

gilit

y Sa

mpl

ing

loca

tions

G

enet

ic

mar

kers

Re

sults

Re

fere

nce

(Com

mon

na

me)

Ca

rcha

rhin

iform

es

Carc

harh

inus

fa

lcifo

rmes

(S

ilky

shar

k)

Circ

umgl

obal

, tr

opic

al w

ater

s Pe

lagi

c (o

cean

ic)

High

G

ulf o

f Cal

iforn

ia,

Paci

fic B

aja

(Mex

ico)

, SW

M

exic

o, C

osta

Ri

ca, E

cuad

or, 2

E

Paci

fic o

cean

ic

regi

ons,

New

Ca

ledo

nia

and

Indo

nesia

mtD

NA

CR

Gen

etic

stru

ctur

e be

twee

n W

Pac

ific

and

E Pa

cific

Oce

an sa

mpl

es (Φ

ST(m

ito)=

0.01

9).

No

gene

tic st

ruct

ure

with

in th

e Ea

st P

acifi

c O

cean

Gal

ván-

Tira

do e

t al

. (20

13)

Pr

iona

ce g

lauc

a

(Blu

e sh

ark)

Ci

rcum

glob

al,

trop

ical

, sub

-tr

opic

al a

nd

tem

pera

te

wat

ers

Pela

gic

(oce

anic

) Hi

gh

10 In

do-W

Pac

ific

loca

tions

m

tDN

A Cy

tB

No

gene

tic st

ruct

ure

Tagu

chi e

t al

. (20

14)

Pr

iona

ce g

lauc

a

(Blu

e sh

ark)

Ci

rcum

glob

al,

trop

ical

, sub

-tr

opic

al a

nd

tem

pera

te

wat

ers

Pela

gic

(oce

anic

) Hi

gh

Indo

nesia

, N

Paci

fic O

cean

, W

Aust

ralia

, E

Aust

ralia

mtD

NA

CR

No

gene

tic st

ruct

ure

Ove

nden

et

al.

(200

9)

Sp

hyrn

a le

win

i (S

callo

ped

ham

mer

head

sh

ark)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

an

d co

asta

l)

High

G

ulf o

f Cal

iforn

ia,

Maz

atla

n (W

M

exic

o), P

acifi

c Co

sta

Rica

, Pac

ific

Pana

ma,

Ecu

ador

mtD

NA

CR a

nd 1

5 m

sats

Ove

rall Φ

ST(m

ito)=

NS,

ove

rall

F ST(m

sat)

=0.0

05. I

BD su

ppor

ted

base

d on

m

tDN

A bu

t not

msa

ts

Nan

ce e

t al

. (20

11)

Chapter 1

26

1

2

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

Ca

rcha

rhin

iform

es

Sphy

rna

lew

ini

(Sca

llope

d ha

mm

erhe

ad

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

an

d co

asta

l)

High

Tr

opic

al E

Pac

ific,

Pa

cific

Pan

ama,

Ha

wai

i, th

e Ph

ilipp

ines

, Ta

iwan

, E

Aust

ralia

, W

Aust

ralia

, Se

yche

lles I

sl.,

Sout

h Af

rica,

W

Afric

a, G

ulf o

f M

exic

o, E

USA

, Br

azil

mtD

NA

CR

Ove

rall Φ

ST(m

ito)=

0.59

8. S

tron

g ge

netic

st

ruct

ure

betw

een

and

acro

ss o

cean

ba

sins,

but

to a

less

er e

xten

t alo

ng

cont

inen

tal m

argi

ns. I

sola

tion

of A

tlant

ic

Oce

an fo

llow

ing

the

rise

of th

e Is

thm

us o

f Pa

nam

a, a

nd su

bseq

uent

disp

ersa

l fro

m

the

Atla

ntic

into

the

Indo

-W P

acifi

c re

gion

du

ring

war

mer

Ple

istoc

ene

perio

ds. E

Pa

cific

pop

ulat

ions

der

ived

from

Indo

-W

Paci

fic re

gion

dur

ing

Late

Ple

istoc

ene

Dunc

an e

t al

. (20

06)

Sphy

rna

lew

ini

(Sca

llope

d ha

mm

erhe

ad

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

an

d co

asta

l)

High

Tr

opic

al E

Pac

ific,

Pa

cific

Pan

ama,

Ha

wai

i, th

e Ph

ilipp

ines

, Ta

iwan

, E

Aust

ralia

, W

Aust

ralia

, Se

yche

lles I

sl.,

Sout

h Af

rica,

W

Afric

a, G

ulf o

f M

exic

o, E

USA

, Br

azil

mtD

NA

CR

Ove

rall Φ

ST(m

ito)=

0.59

8. S

tron

g ge

netic

st

ruct

ure

betw

een

and

acro

ss o

cean

ba

sins,

but

to a

less

er e

xten

t alo

ng

cont

inen

tal m

argi

ns. I

sola

tion

of A

tlant

ic

Oce

an fo

llow

ing

the

rise

of th

e Is

thm

us o

f Pa

nam

a, a

nd su

bseq

uent

disp

ersa

l fro

m

the

Atla

ntic

into

the

Indo

-W P

acifi

c re

gion

du

ring

war

mer

Ple

istoc

ene

perio

ds. E

Pa

cific

pop

ulat

ions

der

ived

from

Indo

-W

Paci

fic re

gion

dur

ing

Late

Ple

istoc

ene

Dun

can

et

al. (

2006

)

Sp

hyrn

a le

win

i (S

callo

ped

ham

mer

head

sh

ark)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

an

d co

asta

l)

High

Tr

opic

al E

Pac

ific,

Pa

cific

Pan

ama,

Ha

wai

i, th

e Ph

ilipp

ines

, Ta

iwan

, E

Aust

ralia

, W

Aust

ralia

, Se

yche

lles I

sl.,

Sout

h Af

rica,

W

Afric

a, G

ulf o

f M

exic

o, E

USA

15 m

sats

an

d co

mpa

-ris

on to

m

tDN

A CR

dat

a fr

om

(200

6)

Ove

rall

F ST(m

sat)=

0.03

5. G

enet

ic st

ruct

ure

betw

een

ocea

n ba

sins,

but

hig

her

conn

ectiv

ity a

long

coa

stlin

es a

nd in

som

e ca

sed

acro

ss o

cean

bas

ins.

Com

paris

on

with

mtD

NA

from

Dun

can

et a

l. (2

006)

in

dica

tes f

emal

e ph

ilopa

try

Daly

-Eng

el

et a

l. (2

012)

27

1


3

Sp

hyrn

a le

win

i (S

callo

ped

ham

mer

head

sh

ark)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

an

d co

asta

l)

High

E

Aust

ralia

, In

done

sia

mtD

NA

NAD

H4

and

8 m

sats

Gen

etic

stru

ctur

e be

twee

n In

done

sia a

nd E

Au

stra

lia b

ased

on

mtD

NA

(pai

rwise

F S

T(mito

)=0.

388-

0.07

3) b

ut n

ot m

sats

. Re

sults

indi

cate

fem

ale

philo

patr

y

Ove

nden

et

al.

(201

1)

Sp

hyrn

a le

win

i sp

. (S

callo

ped

ham

mer

head

sp

.)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

an

d co

asta

l)

High

W

Aus

tral

ia, N

Au

stra

lia,

Indo

nesia

mtD

NA

CR a

nd 3

m

sats

No

gene

tic st

ruct

ure

Ove

nden

et

al.

(200

9)

Ca

rcha

rhin

us

acro

notu

s (B

lack

nose

sh

ark)

E At

lant

ic

Oce

an, t

ropi

cal

and

subt

ropi

cal

wat

ers

Pela

gic

(coa

stal

) Hi

gh

W G

ulf o

f Mex

ico,

E

Gul

f of M

exic

o,

Atla

ntic

US

coas

t, Ba

ham

as, S

Gul

f of

Mex

ico

mtD

NA

CR a

nd 2

3 m

sats

Ove

rall Φ

ST (m

ito)=

0.23

3, o

vera

ll F S

T(msa

t)=0

.015

. All

regi

ons d

iver

ged

afte

r LG

M. S

Gul

f of M

exic

o m

ight

hav

e re

pres

ente

d a

glac

ial r

efug

e

Port

noy

et

al. (

2014

)

Ca

rcha

rhin

us

obsc

urus

(D

usky

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(coa

stal

) Hi

gh

3 re

gion

s: W

At

lant

ic (U

SA),

Sout

h Af

rica,

Au

stra

lia

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

betw

een

W

Atla

ntic

Oce

an, S

outh

Afr

ica

and

Aust

ralia

re

gion

s (Φ

ST(m

ito)=

0.55

). N

o ge

netic

st

ruct

ure

with

in re

gion

s

Bena

vide

s et

al.

(201

1)

Ca

rcha

rhin

us

obsc

urus

(D

usky

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(coa

stal

) Hi

gh

W A

ustr

alia

, E

Aust

ralia

, In

done

sia

mtD

NA

CR a

nd 4

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

Indo

nesia

and

W A

ustr

alia

bas

ed o

n m

tDN

A (Φ

ST(m

ito)=

0.19

1) b

ut n

ot m

sats

. Re

sults

sugg

est f

emal

e ph

ilopa

try

Ove

nden

et

al.

(200

9)

Ca

rcha

rhin

us

brev

ipin

na

(Spi

nner

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers.

Abs

ent

from

the

E Pa

cific

Oce

an

Pela

gic

and

dem

ersa

l (c

oast

al)

High

So

uth

Afric

a, N

Au

stra

lia, E

Au

stra

lia

mtD

NA

NAD

H4

Ove

rall Φ

ST(m

ito)=

0.01

6. G

enet

ic st

ruct

ure

betw

een

Sout

h Af

rica

and

Aust

ralia

(p

airw

ise Φ

ST (m

ito)=

0.02

7-0.

035,

and

so

me

evid

ence

of s

truc

ture

with

in A

ustr

alia

(p

airw

ise Φ

ST(m

ito)=

0.00

7-0.

013)

Ger

aght

y et

al.

(201

3)

Chapter 1

28

1

4

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

Ca

rcha

rhin

iform

es

Ca

rcha

rhin

us

limba

tus

(Bla

cktip

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

and

dem

ersa

l (c

oast

al)

High

Ha

wai

i, Ph

ilipi

nes,

E

Aust

ralia

, W

Aust

ralia

, Ind

ia,

Sout

h Af

rica,

Si

erra

Leo

ne.

Com

paris

on w

ith

sam

ples

from

Ke

eney

et a

l. (2

003)

; Kee

ney

et

al. (

2005

)

mtD

NA

CR

Ove

rall Φ

ST(m

ito)=

0.61

2. S

tron

g ge

netic

st

ruct

ure

betw

een

ocea

n ba

sins,

and

w

ithin

the

Atla

ntic

Oce

an. N

o ge

netic

st

ruct

ure

with

in th

e Pa

cific

Oce

an.

Taxo

nom

ic u

ncer

tain

ty a

bout

W A

tlant

ic C

. lim

batu

s

Keen

ey

and

Heist

(2

006)

Ca

rcha

rhin

us

limba

tus

(Bla

cktip

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

and

dem

ersa

l (c

oast

al)

High

Br

azil,

and

co

mpa

rison

with

sa

mpl

es fr

om

Keen

eyan

d He

ist

(200

6); K

eene

y et

al

. (20

05)

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

(ΦST

(mito

)=0.

64)

betw

een

Braz

il an

d sa

mpl

es fr

om K

eene

y et

al.

(200

3). D

iver

genc

e es

timat

ed ~

1.38

M

ya (M

iddl

e Pl

eist

ocen

e)

Sodr

é et

al

. (20

12)

Ca

rcha

rhin

us

limba

tus

(Bla

cktip

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

and

dem

ersa

l (c

oast

al)

High

N

W A

tlant

ic

Oce

an, G

ulf o

f M

exic

o, Y

ucat

an

peni

nsul

a (M

exic

o), B

elize

(a

ll nu

rser

y ar

eas)

mtD

NA

CR a

nd 8

m

sats

Ove

rall Φ

ST(m

ito)=

0.35

, ove

rall

F ST(m

sat)

=0.0

07. R

esul

ts su

gges

t fem

ale

philo

patr

y

Keen

ey e

t al

. (20

05)

Ca

rcha

rhin

us

mel

anop

teru

s (B

lack

tip

reef

shar

k)

Trop

ical

In

dian

, W a

nd

C Pa

cific

O

cean

s, a

nd

the

E M

edite

rran

ean

Sea

Pela

gic

and

dem

ersa

l (c

oast

al)

Lim

ited

5 Fr

ench

Po

lyne

sian

atol

ls (M

oore

a,

Tetia

roa,

Ra

ngiro

a,

Faka

hina

, Mar

ia)

11 m

sats

G

enet

ic st

ruct

ure

betw

een

all l

ocat

ions

(p

airw

ise F

ST(m

sat)

=0.0

25-0

.148

). Fe

mal

e ph

ilopa

try

sugg

este

d fr

om c

lust

erin

g an

alys

is of

sexe

d sa

mpl

es

Vign

aud

et

al. (

2013

)

Ca

rcha

rhin

us

plum

beus

(S

andb

ar sh

ark)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

and

bent

hic

(coa

stal

an

d oc

eani

c)

High

Ha

wai

i, Ta

iwan

, E

Aust

ralia

, W

Aust

ralia

, W

Atla

ntic

Oce

an

mtD

NA

CR a

nd 8

m

sats

Ove

rall Φ

ST(m

ito)=

0.56

5, o

vera

ll F S

T(msa

t)=0

.050

. Str

ong

gene

tic st

ruct

ure

betw

een

ocea

n ba

sins b

ased

on

mtD

NA

and

msa

ts. G

enet

ic st

ruct

ure

with

in o

cean

ba

sins b

ased

on

mtD

NA

but n

ot m

sats

(w

ith th

e ex

cept

ion

of H

awai

i). D

iver

genc

e be

twee

n At

lant

ic-P

acifi

c O

cean

s, a

nd o

f Ha

wai

i est

imat

ed d

urin

g M

iddl

e Pl

eist

ocen

e. E

vide

nce

of c

onte

mpo

rary

m

ale,

but

not

fem

ale,

gen

e flo

w

Port

noy

et

al. (

2010

)

29

1


5

Ca

rcha

rhin

us

sorr

ah

(Spo

t-ta

il sh

ark)

Indi

an a

nd W

Pa

cific

Oce

ans,

tr

opic

al w

ater

s

Pela

gic

and

dem

ersa

l (c

oast

al)

Lim

ited

W A

ustr

alia

, N

Aust

ralia

, E

Aust

ralia

, In

done

sia

mtD

NA

CR a

nd 5

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

Aust

ralia

n an

d In

done

sian

sam

ples

bas

ed

on m

tDN

A (p

airw

ise Φ

ST(m

ito)=

0.75

1-0.

903)

and

msa

ts (p

airw

ise F

ST(m

sat)=

0.38

-0.

047)

Ove

nden

et

al.

(200

9)

Ca

rcha

rhin

us

sorr

ah

(Spo

t-ta

il sh

ark)

Indi

an a

nd W

Pa

cific

Oce

ans,

tr

opic

al w

ater

s

Pela

gic

and

dem

ersa

l (c

oast

al)

Lim

ited

W A

ustr

alia

, N

Aust

ralia

, E

Aust

ralia

, Cor

al

Sea,

Phi

lippi

nes,

Ta

iwai

n,

Indo

nesia

, Th

aila

nd, I

ndia

, Ar

abia

n G

ulf,

Red

Sea,

Ken

ya

mtD

NA

CR

Ove

rall Φ

ST(m

ito)=

0.73

. Sig

nific

ant g

enet

ic

stru

ctur

e ac

ross

stre

tche

s of d

eep

wat

er,

part

icul

arly

the

Indo

nesia

n Th

roug

hflo

w-

Tim

or P

assa

ge a

nd th

e Co

ral S

ea

Gile

s et a

l. (2

014)

Ca

rcha

rhin

us

ambo

inen

sis

(Pig

-eye

shar

k)

Indo

-W P

acifi

c re

gion

, E

Atla

ntic

O

cean

, M

edite

rra-

nean

Dem

ersa

l (c

oast

al)

Inte

rme-

diat

e W

Aus

tral

ia, N

Au

stra

lia, E

Au

stra

lia, A

rabi

an

Sea,

Sou

th A

fric

a

mtD

NA

CR a

nd

NAD

H4, 4

m

sats

and

nu

clea

r RA

G1

Ove

rall Φ

ST(m

ito)=

0.02

2, o

vera

ll F S

T(msa

t)=N

S. IB

D su

ppor

ted

base

d on

m

tDN

A bu

t not

msa

ts. I

sola

tion

acro

ss

Sund

a/Sa

hul S

helf

durin

g Pl

eist

ocen

e pe

riods

of l

ow se

a le

vels,

follo

wed

by

seco

ndar

y in

trog

ress

ion

durin

g w

arm

er

perio

ds

Tille

tt e

t al

. (20

11)

Ca

rcha

rhin

us

leuc

as

(Bul

l sha

rk)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Dem

ersa

l (c

oast

al

and

fres

hwat

er)

Inte

rme-

diat

e E

Flor

ida,

Gul

f of

Mex

ico,

Bra

zil

mtD

NA

CR a

nd 5

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

Braz

il an

d al

l oth

er lo

catio

ns b

ased

on

mtD

NA

(ΦST

(mito

)=0.

8) b

ut n

ot m

sats

. Res

ults

su

gges

t fem

ale

philo

patr

y

Karl

et a

l. (2

010)

Ca

rcha

rhin

us

leuc

as

(Bul

l sha

rk)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Dem

ersa

l (c

oast

al

and

fres

hwat

er)

Lim

ited

13 N

Aus

tral

ia

river

syst

ems

mtD

NA

CR a

nd

NAD

H4,

and

3 m

sats

Ove

rall Φ

ST(m

ito)=

0.07

7, o

vera

ll F S

T(msa

t)=N

S. R

esul

ts su

gges

t fem

ale

philo

patr

y

Tille

tt e

t al

. (20

12)

M

uste

lus

anta

rtic

us

(Aus

tral

ian

gum

my

shar

k)

S Au

stra

lian

wat

ers

Dem

ersa

l (c

oast

al)

Inte

rme-

diat

e 5

loca

tions

ar

ound

Aus

tral

ia

28

allo

zym

e lo

ci a

nd

mtD

NA

RFLP

Gen

etic

stru

ctur

e be

twee

n S

and

N N

ew

Sout

h W

ales

, and

bet

wee

n To

wns

ville

and

ot

her l

ocat

ions

Gar

dner

an

d W

ard

(199

8)

Chapter 1

30

1

6

Ord

er

Spec

ies n

ame

Dis

trib

utio

n H

abita

t Va

gilit

y Sa

mpl

ing

loca

tions

G

enet

ic

mar

kers

Re

sults

Re

fere

nce

(Com

mon

na

me)

Ca

rcha

rhin

iform

es

Mus

telu

s sc

hmitt

i (N

arro

wno

se

smoo

th-h

ound

sh

ark)

Ende

mic

to S

W

Atla

ntic

O

cean

, te

mpe

rate

w

ater

s

Dem

ersa

l (c

oast

al)

High

Ri

o de

la P

lata

(B

razil

) and

its

Mar

itim

e Fr

ont

mtD

NA

CytB

N

o ge

netic

stru

ctur

e Pe

reyr

a et

al

. (20

10)

N

egap

rion

acut

iden

s (S

ickl

efin

lem

on

shar

k)

Indi

an, W

and

C

Paci

fic

Oce

ans,

tr

opic

al w

ater

s

Dem

ersa

l (c

oast

al)

Lim

ited

Taiw

an, F

renc

h Po

lyne

sia, N

ew

Cale

doni

a, E

Au

stra

lia, W

Au

stra

lia

mtD

NA

CR a

nd 9

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

Taiw

an

and

all o

ther

loca

tions

bas

ed o

n m

tDN

A (Φ

ST(m

ito)=

0.86

). Ta

iwan

and

New

Ca

ledo

nia

not i

nclu

ded

in m

sat a

naly

ses.

G

enet

ic st

ruct

ure

acro

ss re

mai

ning

lo

catio

ns b

ased

on

msa

ts

(θST

(msa

t)=0.

0544

), bu

t not

mtD

NA.

Schu

ltz e

t al

. (20

08)

Rh

izopr

iono

don

lala

ndii

(B

razil

ian

shar

p-no

se sh

ark)

E At

lant

ic

Oce

an, t

ropi

cal

wat

ers

Dem

ersa

l (c

oast

al)

Inte

rme-

diat

e Ca

ribbe

an a

nd S

Br

azil

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

betw

een

Carib

bean

and

Bra

zilia

n sa

mpl

es

(ΦST(m

ito) =

0.254

)

Men

donç

a et

al.

(201

3)

Rh

izopr

iono

don

poro

sus

(Car

ibbe

an

shar

pnos

e sh

ark)

W A

tlant

ic

Oce

an

Dem

ersa

l (c

oast

al

and

brac

kish

w

ater

)

Inte

rme-

diat

e 9

loca

tions

alo

ng

Braz

ilian

coa

st,

Carib

bean

Sea

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

betw

een

loca

tions

no

rth

and

sout

h of

the

Equa

toria

l Cur

rent

(Φ

ST(m

ito)=

0.23

7. IB

D su

ppor

ted

Men

donç

a et

al.

(201

1)

Sc

ylio

rhin

us

cani

cula

(S

mal

l-spo

tted

ca

tsha

rk)

Euro

pean

w

ater

s fro

m

Nor

way

to

Sene

gal,

incl

udin

g th

e M

edite

rra-

nean

Sea

. Te

mpe

rate

an

d su

btro

pica

l w

ater

s

Dem

ersa

l (c

oast

al)

Lim

ited

N N

orw

ay, N

UK,

S

UK,

Por

tuga

l, M

edite

rran

ean

Sea,

Ten

erife

mtD

NA

CR a

nd 1

2 m

sats

Ove

rall Φ

ST(m

ito)=

0.30

8, o

vera

ll F S

T(msa

t)=0

.039

. Str

ong

gene

tic st

ruct

ure

betw

een

Med

iterr

anea

n Se

a an

d al

l oth

er

loca

tions

bas

ed o

n m

tDN

A (p

airw

ise

ΦST

(mito

)=0.

209-

0.60

0) a

nd m

sats

(p

airw

ise F

ST(m

sat)=

0.02

8-0.

057)

. Re

colo

niza

tion

afte

r the

LG

M im

plic

ated

in

lack

of g

enet

ic st

ruct

ure

acro

ss th

e At

lant

ic

shel

f. Re

sults

sugg

estiv

e of

fem

ale

philo

patr

y

Gub

ili e

t al

. (20

14)

31

1


7

Tr

iaki

s se

mifa

scia

ta

(Leo

pard

shar

k)

E Pa

cific

, O

rego

n to

M

exic

o

Dem

ersa

l (c

oast

al)

Inte

rme-

diat

e 10

loca

tions

alo

ng

the

coas

t of

Ore

gon

and

Calif

orni

a

mtD

NA

CR a

nd

nucl

ear

inte

r sim

ple

sequ

ence

re

peat

s (IS

SRs)

Gen

etic

stru

ctur

e al

ong

US

coas

t bas

ed o

n m

tDN

A (Φ

ST(m

ito)=

0.0

69) a

nd n

ucle

ar

ISSR

s (Θ

β (IS

SRs)

=0.1

10).

IBD

supp

orte

d fo

r nu

clea

r ISS

Rs b

ut n

ot m

tDN

A. N

o ev

iden

ce

for s

ex-s

peci

fic p

hilo

patr

y

Lew

alle

n et

al.

(200

7)

Ga

leor

hinu

s ga

leus

(T

ope

shar

k)

Circ

umgl

obal

, te

mpe

rate

w

ater

s

Bent

ho-

pela

gic

(coa

stal

)

High

N

E Pa

cific

, SE

Paci

fic, S

W

Paci

fic, S

W

Atla

ntic

and

NE

Atla

ntic

mtD

NA

CR

Ove

rall Φ

ST(m

ito)=

0.84

0. G

reat

er

diffe

renc

e be

twee

n N

E Pa

cific

and

SE

Paci

fic th

an b

etw

een

NE

Paci

fic a

nd U

K in

dica

tes h

istor

ic tr

ans-

Arct

ic g

ene

flow

du

ring

war

mer

Plio

cene

per

iods

Chab

ot

and

Alle

n (2

009)

N

egap

rion

brev

irost

ris

(Lem

on sh

ark)

Subt

ropi

cal W

At

lant

ic, a

nd

smal

l iso

late

d po

pula

tions

in

the

E At

lant

ic

and

E Pa

cific

O

cean

s

Bent

ho-

pela

gic

(coa

stal

)

Inte

rme-

diat

e E

Paci

fic O

cean

, Ba

ham

as, B

razil

, G

uine

a Bi

ssau

mtD

NA

CR a

nd 9

m

sats

Stro

ng g

enet

ic st

ruct

ure

(ΦST

(mito

)=0.

99,

msa

ts n

ot re

port

ed) b

etw

een

Paci

fic a

nd

Atla

ntic

Oce

ans f

ollo

win

g th

e cl

osur

e of

the

Isth

mus

of P

anam

a (~

3.5

Mya

). St

rong

ge

netic

stru

ctur

e w

ithin

Atla

ntic

Oce

an

base

d on

mtD

NA

(ΦST

(mito

)=0.

92) a

nd

msa

ts (θ

ST(m

sat)

=0.4

7)

Schu

ltz e

t al

. (20

08)

Rh

izopr

iono

don

acut

us

(Milk

shar

k)

Sout

h Af

rican

w

ater

s, In

do-

Wes

t Pac

ific

regi

on a

nd N

Au

stra

lian

wat

ers

Bent

ho-

pela

gic

(coa

stal

)

Unk

now

n E

Aust

ralia

, In

done

sia

mtD

NA

NAD

H4

and

6 m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

Indo

nesia

and

all

othe

r loc

atio

ns b

ased

on

mtD

NA

(pai

rwise

ΦST

(mito

)=0.

568-

0.63

4)

and

msa

ts (p

airw

ise F

ST(m

sat)=

0.16

7-0.

222)

Ove

nden

et

al.

(201

1)

Tr

iaen

odon

ob

esus

(W

hite

tip re

ef

shar

k)

Trop

ical

and

su

btro

pica

l w

ater

s of t

he

Indi

an a

nd

Paci

fic O

cean

s.

Bent

ho-

pela

gic

(coa

stal

)

Lim

ited

Japa

n, E

Indi

an

Oce

an, I

ndon

esia

, Si

ngap

ore,

Gua

m

(W P

acifi

c), N

E Au

stra

lia,

Mar

ques

as

Isla

nds (

C Pa

cific

), Pa

lmyr

a (C

Pa

cific

), Ha

wai

i, Co

cos I

sland

(E

Paci

fic),

Paci

fic

Cost

a Ri

ca

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

betw

een

(ΦST

(mito

)=0.

336)

and

with

in o

cean

bas

ins

(ΦST

(mito

)=0.

336)

, but

hig

h co

nnec

tivity

am

ong

C Pa

cific

Isla

nds.

IBD

supp

orte

d.

Mid

dle

Plei

stoc

ene

expa

nsio

n fr

om a

co

mm

on In

do-W

Pac

ific

ance

stor

su

gges

ted.

Isol

atio

n be

twee

n In

dian

and

Pa

cific

Oce

ans d

urin

g Pl

eist

ocen

e pe

riods

of

low

sea

leve

l

Whi

tney

et

al. (

2012

)

Chapter 1

32

1

8

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

Ca

rcha

rhin

iform

es

Glyp

his g

lyph

is (S

pear

toot

h sh

ark)

N A

ustr

alia

an

d S

Papu

a N

ew G

uine

a,

river

s

Rive

rs

Lim

ited

3 riv

er d

rain

ages

in

N A

ustr

alia

M

G O

vera

ll Φ

ST(m

ito)=

0.28

3. S

tron

g ge

netic

st

ruct

ure

betw

een

all t

hree

rive

r dra

inag

es

(pai

rwise

ΦST

(mito

)=0.

178-

0.53

1)

Feut

ry e

t al

. (20

14)

Lam

nifo

rmes

Al

opia

s pe

lagi

cus

(Pel

agic

th

resh

er sh

ark)

Indi

an a

nd

Paci

fic O

cean

s,

trop

ical

and

su

btro

pica

l w

ater

s

Pela

gic

(oce

anic

) Hi

gh

Sout

hern

Ca

lifor

nia

(USA

), G

ulf o

f Cal

iforn

ia,

Paci

fic C

osta

Ric

a,

Paci

fic C

olom

bia,

G

alap

agos

Isl.,

Cl

ippe

rton

Isl.,

Ha

wai

i, Ta

iwan

mtD

NA

COX1

and

7

msa

ts

Two

reci

proc

ally

mon

ophy

letic

cla

des,

one

pr

esen

t in

all s

ampl

ing

loca

tions

, one

onl

y in

Haw

aii a

nd th

e E

Paci

fic O

cean

. Cla

des

wer

e sig

nific

antly

diff

eren

t bas

ed o

n m

sats

. G

enet

ic st

ruct

ure

betw

een

all l

ocat

ions

ba

sed

on m

tDN

A (p

airw

ise Φ

ST(m

ito)

0.06

2–0.

896)

, but

onl

y be

twee

n th

e W

Pa

cific

and

all

othe

r loc

atio

ns b

ased

on

msa

ts (p

airw

ise F

ST(m

sat)=

0.02

-0.0

75)

Card

eños

a et

al.

(201

4)

Ca

rcha

rodo

n ca

rcha

rias

(Whi

te sh

ark)

Circ

umgo

bal

with

con

cen-

trat

ions

in

tem

pera

te

coas

tal o

cean

s

Pela

gic

(oce

anic

) Hi

gh

4 M

edite

r-ra

nean

in

divi

dual

s,

com

paris

on w

ith

sam

ples

from

Jo

rgen

sen

et a

l. (2

010)

mtD

NA

CR

Med

iterr

anea

n ha

plot

ypes

show

gre

ater

sim

ilarit

y to

Indi

an a

nd P

acifi

c O

cean

s tha

n At

lant

ic O

cean

hap

loty

pes.

Anc

estr

al

conn

ectio

n du

ring

Mid

dle

Plei

stoc

ene

Gub

ili e

t al

. (20

11)

Ca

rcha

rodo

n ca

rcha

rias

(Whi

te sh

ark)

Circ

umgo

bal

with

con

cen-

trat

ions

in

tem

pera

te

coas

tal o

cean

s

Pela

gic

(oce

anic

) Hi

gh

W A

ustr

alia

, S

Aust

ralia

, E

Aust

ralia

, Ta

sman

ia.

Com

paris

on to

se

quen

ces f

rom

Pa

rdin

i et a

l. 20

01, J

orge

nsen

et

al.

2010

and

Gu

bili

et a

l. 20

10

mtD

NA

CR a

nd 6

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

W a

nd E

Au

stra

lia b

ased

on

mtD

NA

(ΦST

(mito

)=0.

142)

and

to a

less

er e

xten

t on

msa

ts (F

ST(m

sat)

=0.0

09).

Evid

ence

of

spor

adic

tran

s-At

lant

ic d

isper

sal b

ased

on

mtD

NA

hapl

otyp

es

Blow

er e

t al

. (20

12)

33

1


8

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

Ca

rcha

rhin

iform

es

Glyp

his g

lyph

is (S

pear

toot

h sh

ark)

N A

ustr

alia

an

d S

Papu

a N

ew G

uine

a,

river

s

Rive

rs

Lim

ited

3 riv

er d

rain

ages

in

N A

ustr

alia

M

G O

vera

ll Φ

ST(m

ito)=

0.28

3. S

tron

g ge

netic

st

ruct

ure

betw

een

all t

hree

rive

r dra

inag

es

(pai

rwise

ΦST

(mito

)=0.

178-

0.53

1)

Feut

ry e

t al

. (20

14)

Lam

nifo

rmes

Al

opia

s pe

lagi

cus

(Pel

agic

th

resh

er sh

ark)

Indi

an a

nd

Paci

fic O

cean

s,

trop

ical

and

su

btro

pica

l w

ater

s

Pela

gic

(oce

anic

) Hi

gh

Sout

hern

Ca

lifor

nia

(USA

), G

ulf o

f Cal

iforn

ia,

Paci

fic C

osta

Ric

a,

Paci

fic C

olom

bia,

G

alap

agos

Isl.,

Cl

ippe

rton

Isl.,

Ha

wai

i, Ta

iwan

mtD

NA

COX1

and

7

msa

ts

Two

reci

proc

ally

mon

ophy

letic

cla

des,

one

pr

esen

t in

all s

ampl

ing

loca

tions

, one

onl

y in

Haw

aii a

nd th

e E

Paci

fic O

cean

. Cla

des

wer

e sig

nific

antly

diff

eren

t bas

ed o

n m

sats

. G

enet

ic st

ruct

ure

betw

een

all l

ocat

ions

ba

sed

on m

tDN

A (p

airw

ise Φ

ST(m

ito)

0.06

2–0.

896)

, but

onl

y be

twee

n th

e W

Pa

cific

and

all

othe

r loc

atio

ns b

ased

on

msa

ts (p

airw

ise F

ST(m

sat)=

0.02

-0.0

75)

Card

eños

a et

al.

(201

4)

Ca

rcha

rodo

n ca

rcha

rias

(Whi

te sh

ark)

Circ

umgo

bal

with

con

cen-

trat

ions

in

tem

pera

te

coas

tal o

cean

s

Pela

gic

(oce

anic

) Hi

gh

4 M

edite

r-ra

nean

in

divi

dual

s,

com

paris

on w

ith

sam

ples

from

Jo

rgen

sen

et a

l. (2

010)

mtD

NA

CR

Med

iterr

anea

n ha

plot

ypes

show

gre

ater

sim

ilarit

y to

Indi

an a

nd P

acifi

c O

cean

s tha

n At

lant

ic O

cean

hap

loty

pes.

Anc

estr

al

conn

ectio

n du

ring

Mid

dle

Plei

stoc

ene

Gub

ili e

t al

. (20

11)

Ca

rcha

rodo

n ca

rcha

rias

(Whi

te sh

ark)

Circ

umgo

bal

with

con

cen-

trat

ions

in

tem

pera

te

coas

tal o

cean

s

Pela

gic

(oce

anic

) Hi

gh

W A

ustr

alia

, S

Aust

ralia

, E

Aust

ralia

, Ta

sman

ia.

Com

paris

on to

se

quen

ces f

rom

Pa

rdin

i et a

l. 20

01, J

orge

nsen

et

al.

2010

and

Gu

bili

et a

l. 20

10

mtD

NA

CR a

nd 6

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

W a

nd E

Au

stra

lia b

ased

on

mtD

NA

(ΦST

(mito

)=0.

142)

and

to a

less

er e

xten

t on

msa

ts (F

ST(m

sat)

=0.0

09).

Evid

ence

of

spor

adic

tran

s-At

lant

ic d

isper

sal b

ased

on

mtD

NA

hapl

otyp

es

Blow

er e

t al

. (20

12)

9

Ca

rcha

rodo

n ca

rcha

rias

(Whi

te sh

ark)

Circ

umgo

bal

with

co

ncen

tra-

tions

in

tem

pera

te

coas

tal o

cean

s

Pela

gic

(oce

anic

) Hi

gh

NE

Paci

fic,

Aust

ralia

/New

Ze

alan

d, S

outh

Af

rica

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

betw

een

all

loca

tions

(pai

rwise

FST

(mito

)=0.

68-0

.97)

. An

cest

ral c

onne

ctio

n be

twee

n N

E Pa

cific

an

d Au

stra

lia/N

ew Z

eala

nd d

ated

to th

e La

te P

leist

ocen

e

Jorg

ense

n et

al.

(201

0)

Ca

rcha

rodo

n ca

rcha

rias

(Whi

te sh

ark)

Circ

umgo

bal

with

co

ncen

tra-

tions

in

tem

pera

te

coas

tal o

cean

s

Pela

gic

(oce

anic

) Hi

gh

Aust

ralia

, New

Ze

alan

d, S

outh

Af

rica

mtD

NA

CR a

nd 5

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

Sout

h Af

rica

and

othe

r loc

atio

ns b

ased

on

mtD

NA

(pai

rwise

FST

(mito

)=0.

810-

0.89

0) b

ut n

ot

msa

ts. R

esul

ts su

gges

t fem

ale

philo

patr

y

Pard

ini e

t al

. (20

01)

Ce

torh

inus

m

axim

us

(Bas

king

shar

k)

Circ

umgl

obal

, te

mpe

rate

w

ater

s

Pela

gic

(oce

anic

) Hi

gh

Med

iterr

anea

n Se

a, N

W A

tlant

ic,

NE

Atla

ntic

, In

dian

and

W

Paci

fic O

cean

s

mtD

NA

CR

No

gene

tic st

ruct

ure

Hoel

zel e

t al

. (20

06)

Is

urus

ox

yrin

chus

(S

hort

fin m

ako)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

) Hi

gh

N A

tlant

ic, S

At

lant

ic, N

Pac

ific,

S

Paci

fic, S

outh

Af

rica

Re-

anal

ysis

of

RFLP

dat

a fr

om

Heist

et

al. (

1996

) an

d 4

msa

ts

Lim

ited

gene

tic st

ruct

ure

base

d on

msa

ts.

Com

paris

on to

mtD

NA

from

Hei

st e

t al.

(199

6) in

dica

tes f

emal

e ph

ilopa

try

Schr

ey a

nd

Heist

(2

003)

Ca

rcha

rias

taur

us

(Gre

y nu

rse

shar

k)

Trop

ical

and

su

btro

pica

l w

ater

s, e

xcep

t th

e E

Paci

fic

Oce

an

Pela

gic

and

dem

ersa

l (c

oast

al)

Inte

rme-

diat

e E

Aust

ralia

, Jap

an,

W A

ustr

alia

, So

uth

Afric

a, N

W

Atla

ntic

, Bra

zil

mtD

NA

CR a

nd 6

m

sats

Stro

ng g

enet

ic st

ruct

ure

betw

een

all

loca

tions

bas

ed o

n m

tDN

A (p

airw

ise

F ST(m

ito)=

0.16

3-1.

000)

and

msa

ts (p

airw

ise

F ST(m

sat)=

0.03

2-0.

669)

. Pai

rwise

co

mpa

rison

s with

in A

tlant

ic O

cean

NS.

Sh

ared

hap

loty

pes b

etw

een

Braz

il an

d So

uth

Afric

a in

dica

tes a

rela

tivel

y re

cent

(P

leist

ocen

e) c

onne

ctio

n

Ahon

en e

t al

. (20

09)

Chapter 1

34

1

10

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

O

rect

olob

iform

es

Rhin

codo

n ty

pus

(Wha

le sh

ark)

Ci

rcum

glob

al,

trop

ical

and

su

btro

pica

l w

ater

s

Pela

gic

(oce

anic

) Hi

gh

W A

ustr

alia

, NW

Pa

cific

, NE

Pacf

ic,

W In

dian

Oce

an,

NW

Atla

ntic

mtD

NA

CR

Ove

rall Φ

ST(m

ito)=

0.10

7. S

tron

g ge

netic

di

ffere

ntia

tion

betw

een

Atla

ntic

, Ind

ian

and

Paci

fic O

cean

s. H

igh

conn

ectiv

ity

with

in o

cean

bas

ins.

Pos

sible

disp

ersa

l be

twee

n At

lant

ic a

nd In

dian

Oce

ans d

urin

g hi

atus

of c

old

Beng

uela

upw

ellin

g du

ring

the

Plei

stoc

ene

Cast

ro e

t al

. (20

07)

Rh

inco

don

typu

s (W

hale

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

) Hi

gh

Red

Sea,

Se

yche

lles,

M

ozam

biqu

e, W

Au

stra

lia, G

ulf o

f Ca

lifor

nia,

Gul

f of

Mex

ico,

Mal

dive

s Is

l., P

hilip

pine

s

mtD

NA

CR a

nd 1

4 m

sats

Ove

rall Φ

ST(m

ito)=

0.07

5, o

vera

ll F S

T(msa

t)=0

.021

. Str

ong

gene

tic st

ruct

ure

betw

een

Indo

-Pac

ific

and

Atla

ntic

po

pula

tions

for m

tDN

A (p

airw

ise

ΦST

(mito

)=0.

194-

0.35

1) a

nd m

sats

(p

airw

ise F

ST(m

sat)=

0.01

3-0.

030)

. No

gene

tic st

ruct

ure

with

in o

cean

bas

ins

Vign

aud

et

al. (

2014

)

St

egos

tom

a fa

scia

tum

(Z

ebra

shar

k)

Indo

-W P

acifi

c re

gion

De

mer

sal

and

bent

hic

(coa

stal

)

Inte

rme-

diat

e Au

stra

lia, P

apua

N

ew G

uine

a,

Indo

nesia

, Bo

rneo

, Tha

iland

, Ja

pan,

Sou

th

Afric

a

mtD

NA

NAD

H4

and

13

msa

ts

Ove

rall Φ

ST(m

ito)=

0.53

9, o

vera

ll F S

T(msa

t)=0

.061

. The

Indo

nesia

n Th

roug

hflo

w-T

imor

Pas

sage

mig

ht a

ct a

s a

barr

ier t

o di

sper

sal

Dudg

eon

et a

l. (2

009)

Gi

ngly

mos

tom

a ci

rrat

um (N

urse

sh

ark)

Atla

ntic

and

Ea

ster

n Pa

cific

O

cean

s,

trop

ical

wat

ers

Dem

ersa

l an

d be

nthi

c (c

oast

al)

Lim

ited

Gul

f of M

exic

o,

Baha

mas

, Bel

ize,

2 of

fsho

re

Braz

ilian

Isl.

mtD

NA

CR a

nd 8

m

sats

Ove

rall

F ST(m

ito)=

0.78

2, o

vera

ll F S

T(msa

t)=N

R. S

tron

g ge

netic

stru

ctur

e be

twee

n Br

azil

and

all o

ther

sam

ples

bas

ed

on m

tDN

A (F

ST(m

ito)=

0.10

9-0.

334)

and

m

sats

(FST

(msa

t)=0.

009-

0.03

0)

Karl

et a

l. (2

011)

Myl

ioba

tifor

mes

Ae

toba

tus

narin

ari (

Whi

te-

spot

ted

eagl

e ra

y)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic,

de

mer

sal

and

bent

hic

(coa

stal

)

Unk

now

n E

Paci

fic O

cean

, Ha

wai

i, In

done

sia,

Sout

h Ch

ina

Sea,

Ja

pan,

E A

tlant

ic

Oce

an

mtD

NA

CytB

and

CO

X1, a

nd

nucl

ear

ITS2

E Pa

cific

, Atla

ntic

and

oth

er P

acifi

c sa

mpl

es

cons

ist o

f rec

ipro

cally

mon

ophy

letic

lin

eage

s, p

roba

bly

repr

esen

ting

thre

e se

para

te (s

ub)s

peci

es. D

iver

genc

es

estim

ated

bet

wee

n 5.

7 an

d 3.

4 M

ya

Rich

ards

et

al. (

2009

)

35

1


10

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

O

rect

olob

iform

es

Rhin

codo

n ty

pus

(Wha

le sh

ark)

Ci

rcum

glob

al,

trop

ical

and

su

btro

pica

l w

ater

s

Pela

gic

(oce

anic

) Hi

gh

W A

ustr

alia

, NW

Pa

cific

, NE

Pacf

ic,

W In

dian

Oce

an,

NW

Atla

ntic

mtD

NA

CR

Ove

rall Φ

ST(m

ito)=

0.10

7. S

tron

g ge

netic

di

ffere

ntia

tion

betw

een

Atla

ntic

, Ind

ian

and

Paci

fic O

cean

s. H

igh

conn

ectiv

ity

with

in o

cean

bas

ins.

Pos

sible

disp

ersa

l be

twee

n At

lant

ic a

nd In

dian

Oce

ans d

urin

g hi

atus

of c

old

Beng

uela

upw

ellin

g du

ring

the

Plei

stoc

ene

Cast

ro e

t al

. (20

07)

Rh

inco

don

typu

s (W

hale

shar

k)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic

(oce

anic

) Hi

gh

Red

Sea,

Se

yche

lles,

M

ozam

biqu

e, W

Au

stra

lia, G

ulf o

f Ca

lifor

nia,

Gul

f of

Mex

ico,

Mal

dive

s Is

l., P

hilip

pine

s

mtD

NA

CR a

nd 1

4 m

sats

Ove

rall Φ

ST(m

ito)=

0.07

5, o

vera

ll F S

T(msa

t)=0

.021

. Str

ong

gene

tic st

ruct

ure

betw

een

Indo

-Pac

ific

and

Atla

ntic

po

pula

tions

for m

tDN

A (p

airw

ise

ΦST

(mito

)=0.

194-

0.35

1) a

nd m

sats

(p

airw

ise F

ST(m

sat)=

0.01

3-0.

030)

. No

gene

tic st

ruct

ure

with

in o

cean

bas

ins

Vign

aud

et

al. (

2014

)

St

egos

tom

a fa

scia

tum

(Z

ebra

shar

k)

Indo

-W P

acifi

c re

gion

De

mer

sal

and

bent

hic

(coa

stal

)

Inte

rme-

diat

e Au

stra

lia, P

apua

N

ew G

uine

a,

Indo

nesia

, Bo

rneo

, Tha

iland

, Ja

pan,

Sou

th

Afric

a

mtD

NA

NAD

H4

and

13

msa

ts

Ove

rall Φ

ST(m

ito)=

0.53

9, o

vera

ll F S

T(msa

t)=0

.061

. The

Indo

nesia

n Th

roug

hflo

w-T

imor

Pas

sage

mig

ht a

ct a

s a

barr

ier t

o di

sper

sal

Dudg

eon

et a

l. (2

009)

Gi

ngly

mos

tom

a ci

rrat

um (N

urse

sh

ark)

Atla

ntic

and

Ea

ster

n Pa

cific

O

cean

s,

trop

ical

wat

ers

Dem

ersa

l an

d be

nthi

c (c

oast

al)

Lim

ited

Gul

f of M

exic

o,

Baha

mas

, Bel

ize,

2 of

fsho

re

Braz

ilian

Isl.

mtD

NA

CR a

nd 8

m

sats

Ove

rall

F ST(m

ito)=

0.78

2, o

vera

ll F S

T(msa

t)=N

R. S

tron

g ge

netic

stru

ctur

e be

twee

n Br

azil

and

all o

ther

sam

ples

bas

ed

on m

tDN

A (F

ST(m

ito)=

0.10

9-0.

334)

and

m

sats

(FST

(msa

t)=0.

009-

0.03

0)

Karl

et a

l. (2

011)

Myl

ioba

tifor

mes

Ae

toba

tus

narin

ari (

Whi

te-

spot

ted

eagl

e ra

y)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic,

de

mer

sal

and

bent

hic

(coa

stal

)

Unk

now

n E

Paci

fic O

cean

, Ha

wai

i, In

done

sia,

Sout

h Ch

ina

Sea,

Ja

pan,

E A

tlant

ic

Oce

an

mtD

NA

CytB

and

CO

X1, a

nd

nucl

ear

ITS2

E Pa

cific

, Atla

ntic

and

oth

er P

acifi

c sa

mpl

es

cons

ist o

f rec

ipro

cally

mon

ophy

letic

lin

eage

s, p

roba

bly

repr

esen

ting

thre

e se

para

te (s

ub)s

peci

es. D

iver

genc

es

estim

ated

bet

wee

n 5.

7 an

d 3.

4 M

ya

Rich

ards

et

al. (

2009

)

11

Ae

toba

tus

narin

ari (

Whi

te-

spot

ted

eagl

e ra

y)

Circ

umgl

obal

, tr

opic

al a

nd

subt

ropi

cal

wat

ers

Pela

gic,

de

mer

sal

and

bent

hic

(coa

stal

)

Unk

now

n W

Aus

tral

ia, N

Au

stra

lia, E

Au

stra

lia,

Indo

nesia

, M

alay

sia,

Thai

land

, Sou

th

Chin

a Se

a, H

ong

Kong

, Tai

wan

, Ja

pan,

Sou

th

Afric

a, P

uert

o Ri

co, F

lorid

a.

Com

paris

on to

sa

mpl

es fr

om

Rich

ards

et a

l. 20

09

mtD

NA

CytB

and

N

ADH4

Ove

rall Φ

ST(m

ito)=

0.82

and

0.9

4, C

ytB

and

NAD

H4 re

spec

tivel

y. L

imite

d co

nnec

tivity

be

twee

n Ea

st C

hina

Sea

, Sou

thea

st A

sia

and

Aust

ralia

. Pos

sible

cry

ptic

spec

iatio

n du

ring

Late

/Mid

dle

Plei

stoc

ene

is th

ough

t to

resu

lt fr

om li

mite

d di

sper

sal,

rath

er th

an

vica

rianc

e ac

ross

Ple

istoc

ene

barr

iers

to

disp

ersa

l

Schl

uess

el

et a

l. (2

010)

Da

syat

is ak

ajei

(R

ed st

ingr

ay)

NW

Pac

ific

Oce

an, t

ropi

cal

and

subt

ropi

cal

wat

ers

Dem

ersa

l an

d be

nthi

c (c

oast

al)

Unk

now

n Ja

pan,

and

6

loca

tions

alo

ng

the

coas

t of C

hina

207

AFLP

lo

ci

Ove

rall Φ

ST(A

FLP)

=0.0

58. G

enet

ic st

ruct

ure

betw

een

all s

ampl

ing

loca

tions

(pai

rwise

F S

T(AFL

P)=0

.046

-0.1

15)

Li e

t al.

(201

3)

Za

pter

yx

exas

pera

ta

(Ban

ded

guita

rfish

)

E Pa

cific

O

cean

, tro

pica

l an

d su

btro

pica

l w

ater

s

Dem

ersa

l an

d be

nthi

c (c

oast

al)

Lim

ited

NE

and

SE G

ulf o

f Ca

lifor

nia,

and

N

W a

nd C

W B

aja

Peni

nsul

a (P

acifi

c O

cean

)

mtD

NA

NAD

H2

and

CR

Ove

rall Φ

ST(m

ito)=

0.16

0 an

d 0.

42 fo

r N

ADH2

and

CR

resp

ectiv

ely.

Gen

etic

st

ruct

ure

betw

een

Gul

f of C

alifo

rnia

(p

airw

ise Φ

ST(m

ito)=

0.20

9-0.

337

and

0.39

1-0.

481

for N

ADH2

and

CR

resp

ectiv

ely)

Cast

illo-

Paez

et a

l. (2

014)

Rh

inop

tera

st

eind

achn

eri

(Gol

den

cow

nose

ray)

E Pa

cific

O

cean

, tro

pica

l an

d su

btro

pica

l w

ater

s

Pela

gic,

de

mer

sal

and

bent

hic

(coa

stal

)

High

G

ulf o

f Cal

iforn

ia,

Paci

fic M

exic

o m

tDN

A N

ADH2

O

vera

ll Φ

ST(m

ito)=

0.97

2. P

ossib

le c

rypt

ic

spec

iatio

n be

twee

n th

e G

ulf o

f Cal

iforn

ia

and

the

Paci

fic O

cean

Sand

oval

-Ca

still

o an

d Ro

cha-

Oliv

ares

(2

011)

Chapter 1

36

1

12

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

M

ylio

batif

orm

es

Dasy

atis

brev

icau

data

(S

hort

-tai

led

stin

gray

)

Sout

hern

He

misp

here

, te

mpe

rate

w

ater

s

Dem

ersa

l an

d be

nthi

c (c

oast

al)

Lim

ited

New

Zea

land

, W

Aust

ralia

, E

Aust

ralia

and

So

uth

Afric

a

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

betw

een

New

Ze

alan

d, A

ustr

alia

and

Sou

th A

fric

a re

gion

s (Φ

ST(m

ito)=

0.67

0). I

BD su

ppor

ted.

Di

sper

sal b

etw

een

Aust

ralia

and

New

Ze

alan

d du

e to

low

sea

leve

ls du

ring

LGM

. So

uth

Afric

a lin

eage

div

erge

d ea

rlier

, du

ring

Mid

dle

Plei

stoc

ene

Le P

ort

and

Lave

ry

(201

2)

N

eotr

ygon

kuh

lii

(Blu

e-sp

otte

d m

askr

ay)

Indo

-W P

acifi

c re

gion

, tr

opic

al w

ater

s

Bent

hic

(coa

stal

) Li

mite

d 26

loca

tions

in

the

Cora

l Tria

ngle

m

tDN

A CO

X1

7 di

stin

ct c

lade

s with

exc

lusiv

e ge

ogra

phic

di

strib

utio

ns (Φ

ST(m

ito)=

0.65

5). S

tron

g ge

netic

stru

ctur

e be

twee

n po

pula

tions

w

ithin

cla

des (Φ

ST(m

ito)=

0.24

7)

Arly

za e

t al

. (20

13)

U

roba

tis h

alle

ri

(Rou

nd st

ingr

ay)

E Pa

cific

, O

rego

n to

Pa

nam

a

Bent

hic

(coa

stal

) Li

mite

d Co

asta

l Cal

iforn

ia,

Cata

lina

Isl.

(Cal

iforn

ia) a

nd

the

Gul

f of

Calif

orni

a

7 m

sats

G

enet

ic st

ruct

ure

betw

een

Cata

lina

Isl.

and

othe

r loc

atio

ns. D

eep

wat

er m

ight

act

as a

ba

rrie

r to

gene

flow

Plan

k et

al.

(201

0)

Prist

iform

es

Rhin

obat

os

prod

uctu

s (S

hove

lnos

e gu

itarf

ish)

E Pa

cific

O

cean

, su

btro

pica

l w

ater

s

Bent

hic

(coa

stal

) Li

mite

d G

ulf o

f Cal

iforn

ia,

Paci

fic M

exic

o m

tDN

A CR

O

vera

ll Φ

ST(m

ito)=

0.63

. Pos

sible

cry

ptic

sp

ecia

tion

betw

een

the

Gul

f of C

alifo

rnia

an

d Pa

cific

Mex

ico.

Div

erge

nce

estim

ated

ar

ound

3.1

Mya

Sand

oval

-Ca

still

o et

al

. (20

04)

Rajif

orm

es

Ambl

yraj

a ra

diat

a

(Tho

rny

skat

e)

N A

tlant

ic

Oce

an, N

orth

Se

a, B

altic

Sea

Bent

hic

(coa

stal

) Li

mite

d N

ewfo

undl

and,

W

Icel

and,

N

Icel

and,

E Ic

elan

d,

Nor

th S

ea,

Katt

egat

, W

Nor

way

mtD

NA

CytB

O

vera

ll θ(

mito

)=0.

019.

Gen

etic

stru

ctur

e be

twee

n Ka

tteg

at a

nd m

ost o

ther

loca

tions

(p

airw

ise θ

(mito

)=0.

037-

0.10

1). N

o ge

netic

st

ruct

ure

afte

r rem

oval

of K

atte

gat

sam

ples

. LG

M h

ad li

ttle

effe

ct o

n ge

netic

st

ruct

ure

Chev

olot

et

al.

(200

7)

37

1


12

Ord

er

Spec

ies n

ame

Dist

ribut

ion

Hab

itat

Vagi

lity

Sam

plin

g lo

catio

ns

Gen

etic

m

arke

rs

Resu

lts

Refe

renc

e

(Com

mon

na

me)

M

ylio

batif

orm

es

Dasy

atis

brev

icau

data

(S

hort

-tai

led

stin

gray

)

Sout

hern

He

misp

here

, te

mpe

rate

w

ater

s

Dem

ersa

l an

d be

nthi

c (c

oast

al)

Lim

ited

New

Zea

land

, W

Aust

ralia

, E

Aust

ralia

and

So

uth

Afric

a

mtD

NA

CR

Stro

ng g

enet

ic st

ruct

ure

betw

een

New

Ze

alan

d, A

ustr

alia

and

Sou

th A

fric

a re

gion

s (Φ

ST(m

ito)=

0.67

0). I

BD su

ppor

ted.

Di

sper

sal b

etw

een

Aust

ralia

and

New

Ze

alan

d du

e to

low

sea

leve

ls du

ring

LGM

. So

uth

Afric

a lin

eage

div

erge

d ea

rlier

, du

ring

Mid

dle

Plei

stoc

ene

Le P

ort

and

Lave

ry

(201

2)

N

eotr

ygon

kuh

lii

(Blu

e-sp

otte

d m

askr

ay)

Indo

-W P

acifi

c re

gion

, tr

opic

al w

ater

s

Bent

hic

(coa

stal

) Li

mite

d 26

loca

tions

in

the

Cora

l Tria

ngle

m

tDN

A CO

X1

7 di

stin

ct c

lade

s with

exc

lusiv

e ge

ogra

phic

di

strib

utio

ns (Φ

ST(m

ito)=

0.65

5). S

tron

g ge

netic

stru

ctur

e be

twee

n po

pula

tions

w

ithin

cla

des (Φ

ST(m

ito)=

0.24

7)

Arly

za e

t al

. (20

13)

U

roba

tis h

alle

ri

(Rou

nd st

ingr

ay)

E Pa

cific

, O

rego

n to

Pa

nam

a

Bent

hic

(coa

stal

) Li

mite

d Co

asta

l Cal

iforn

ia,

Cata

lina

Isl.

(Cal

iforn

ia) a

nd

the

Gul

f of

Calif

orni

a

7 m

sats

G

enet

ic st

ruct

ure

betw

een

Cata

lina

Isl.

and

othe

r loc

atio

ns. D

eep

wat

er m

ight

act

as a

ba

rrie

r to

gene

flow

Plan

k et

al.

(201

0)

Prist

iform

es

Rhin

obat

os

prod

uctu

s (S

hove

lnos

e gu

itarf

ish)

E Pa

cific

O

cean

, su

btro

pica

l w

ater

s

Bent

hic

(coa

stal

) Li

mite

d G

ulf o

f Cal

iforn

ia,

Paci

fic M

exic

o m

tDN

A CR

O

vera

ll Φ

ST(m

ito)=

0.63

. Pos

sible

cry

ptic

sp

ecia

tion

betw

een

the

Gul

f of C

alifo

rnia

an

d Pa

cific

Mex

ico.

Div

erge

nce

estim

ated

ar

ound

3.1

Mya

Sand

oval

-Ca

still

o et

al

. (20

04)

Rajif

orm

es

Ambl

yraj

a ra

diat

a

(Tho

rny

skat

e)

N A

tlant

ic

Oce

an, N

orth

Se

a, B

altic

Sea

Bent

hic

(coa

stal

) Li

mite

d N

ewfo

undl

and,

W

Icel

and,

N

Icel

and,

E Ic

elan

d,

Nor

th S

ea,

Katt

egat

, W

Nor

way

mtD

NA

CytB

O

vera

ll θ(

mito

)=0.

019.

Gen

etic

stru

ctur

e be

twee

n Ka

tteg

at a

nd m

ost o

ther

loca

tions

(p

airw

ise θ

(mito

)=0.

037-

0.10

1). N

o ge

netic

st

ruct

ure

afte

r rem

oval

of K

atte

gat

sam

ples

. LG

M h

ad li

ttle

effe

ct o

n ge

netic

st

ruct

ure

Chev

olot

et

al.

(200

7)

13

Ra

ja c

lava

ta

(Tho

rnba

ck ra

y)

E At

lant

ic

Oce

an,

Med

iterr

a-ne

an S

ea,

Blac

k Se

a.

Unc

erta

in

taxo

nom

ic

stat

us in

Sou

th

Afric

a an

d W

In

dian

Oce

an

Dem

ersa

l an

d be

nthi

c (c

oast

al)

Lim

ited

Nor

th S

ea/E

nglis

h Ch

anne

l/Iris

h Se

a,

Gul

f of B

iscay

, Po

rtug

al

Med

iterr

anea

n Se

a, B

lack

Sea

an

d Az

ores

Is

land

s

mtD

NA

CytB

and

5

msa

ts

Ove

rall

θ(m

ito)=

0.34

8, o

vera

ll θ(

msa

ts)=

0.04

7. P

airw

ise c

ompa

rison

s su

gges

t gen

etic

stru

ctur

e be

twee

n Az

ores

Is

l., A

tlant

ic c

ontin

enta

l she

lf an

d M

edite

rran

ean/

Blac

k Se

a re

gion

s, b

ased

on

both

mtD

NA

and

msa

ts. I

BD su

ppor

ted.

Br

itish

wat

ers a

re se

cond

ary

cont

act z

one,

re

colo

nize

d fr

om th

e Ib

eria

n Pe

nins

ula/

Azor

es Is

l. re

gion

aft

er th

e LG

M

Chev

olot

et

al.

(200

6)

Squa

lifor

mes

Ce

ntro

scym

nus

crep

idat

er

(Lon

g-no

sed

velv

et d

ogfis

h)

E At

lant

ic,

Indi

an O

cean

, W

Pac

ific,

SE

Paci

fic O

cean

s,

bath

yal (

deep

) w

ater

s

Dem

ersa

l an

d be

nthi

c (d

eep

wat

er)

Unk

now

n At

lant

ic O

cean

, S

Paci

fic O

cean

, Ta

sman

Sea

mtD

NA

CR a

nd 7

m

sats

Gen

etic

stru

ctur

e be

twee

n At

lant

ic a

nd

Paci

fic O

cean

s bas

ed o

n m

sats

(F

ST(m

sat)=

0.05

) but

not

mtD

NA,

due

to th

e pr

esen

ce o

f tw

o de

eply

div

erge

nt m

tDN

A lin

eage

with

equ

al fr

eque

ncie

s in

both

oc

ean

basin

s. A

llopa

tric

div

erge

nce

date

d ~1

5 M

ya (M

ioce

ne).

No

gene

tic st

ruct

ure

with

in o

cean

bas

ins b

ased

on

both

mtD

NA

and

msa

ts

Cunh

a et

al

. (20

12)

Sq

uatin

a ca

lifor

nica

(P

acifi

c an

gel

shar

k)

E Pa

cific

O

cean

, te

mpe

rate

w

ater

s

Bent

hic

Lim

ited

N C

hann

el Is

land

s an

d S

Chan

nel

Isla

nds

(Cal

iforn

ia, U

SA)

7 allo

zym

e lo

ci

Ove

rall

θ(al

lozy

me)

=0.0

82. G

enet

ic

stru

ctur

e be

twee

n N

and

S C

hann

el Is

land

s.

Deep

wat

er m

ay a

ct a

s a b

arrie

r to

disp

ersa

l

Gai

da

(199

7)

University of Groningen Genetics of manta and devil rays ...Chapter 1 10 Figure 2: Bayesian...

Documents

Transcript of University of Groningen Genetics of manta and devil rays ...Chapter 1 10 Figure 2: Bayesian...