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Mar Biol (2015) 162:2291–2303DOI 10.1007/s00227-015-2759-9

ORIGINAL PAPER

Adaptive radiation of damselfishes (Perciformes, Pomacentridae) in the eastern Pacific

Rosalía Aguilar‑Medrano1,2 · Héctor Reyes‑Bonilla3 · P. David Polly4

Received: 8 July 2015 / Accepted: 5 October 2015 / Published online: 23 October 2015 © Springer-Verlag Berlin Heidelberg 2015

damselfishes: in islands, the distance of the island to the mainland and the size of the island; while in the mainland, the temperature appears to be the main barrier. Our results show the radiation process of Pomacentridae in the eastern Pacific as a dynamic dispersion system, which can be cat-egorized in three main steps: (1) mixture and speciation of species with close affinity to west Atlantic ancestral stocks in the Central Province, (2) dispersion due to favorable conditions to Galapagos islands and Gulf of California and (3) the more complex and perhaps long, gradual dispersal and radiation to temperate areas and isolated or marginal environments.

Introduction

While the earliest divergences among perciform fishes may have occurred in the rudist-dominated Cretaceous car-bonate platforms during the fragmentation of Gondwana (about 75 My) (Kauffman and Fagerstrom 1993; Bellwood et al. 2004), the radiation of the Pomacentridae and other reef fish families was closely associated with the re-emer-gence of coral reefs in the early Eocene during the Ceno-zoic climatic optimum (about 50 My) and the explosion of these ecosystems that continued into the Neogene. With the closure of the Tethys about 18–19 My and the diver-sification of coral reefs in the tectonically dynamic area between Australia and mainland Asia just prior to that time, the center of diversity shifted from the Mediterranean to the Indo-West Pacific (Williams and Duda 2008; Kiessling 2009). The Pomacentridae family is closely related to the Indo-West Pacific (Allen and Robertson 1998; Drew and Barber 2009), which has been identified by several stud-ies as an evolutionary diversity hot spot (Briggs 1992; 1999; Bellwood and Hughes 2001; Streelman et al. 2002;

Abstract Pomacentridae is one of the most abundant families in tropical and temperate rocky and coral reefs. They present an extraordinary diversity of habitat prefer-ences, feeding, morphologies and behavior. The eastern Pacific is biogeographically isolated by the Isthmus of Panama and the eastern Pacific barrier. There is an agree-ment about the origin of the fauna of the Tropical Eastern Pacific, suggesting three main factors, mixture, disper-sal and vicariance. In this study, by cluster analyses and parsimony analysis of endemism, the distribution of dam-selfishes within the eastern Pacific was analyzed to elu-cidate the provinciality and the history of their radiation. Six main provinces were found: (1) Easter Pacific equato-rial islands, (2) North, (3) Center, (4) South, (5) Califor-nia Province and (6) Clipperton. The Gulf of California and Galapagos islands are the two main centers of spe-cies richness. Three main factors limited the radiation of

Responsible Editor: M. Taylor.

Reviewed by X. Moreno and an undisclosed expert.

* Rosalía Aguilar-Medrano liabiol@gmail.com

1 Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 621 Charles E. Young Dr. South, Los Angeles, CA 90095, USA

2 Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas, 356 División del Golfo, Col. Libertad, 87029 Ciudad Victoria, Tamaulipas, Mexico

3 Departamento Académico de Biología Marina, Universidad Autónoma de Baja California Sur, La Paz, BCS, Mexico

4 Department of Geological Sciences, Biology, and Anthropology, Indiana University, 1001 E. 10th Street, Bloomington, IN 47405, USA

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Williams and Duda 2008; Cowman and Bellwood 2012; Kulbicki et al. 2013).

Pomacentridae, a group of marine fishes found in tropi-cal and temperate waters, is one of the most abundant fami-lies in rocky and coral reefs. They present an extraordinary diversity of habitat preferences, feeding, morphology, behavior and color pattern (Allen and Robertson 1998). The monophyly of this family has been demonstrated by both morphological (Stiassny 1981; Kaufman and Liem 1982; Lauder and Liem 1983) and molecular analyses (Tang 2001; Quenouille et al. 2004; Cooper et al. 2009; Frederich et al. 2013). Molecular phylogenies have found segregation into five clades: (1) Lepidozyginae: one mono-specific genus; (2) Stegastinae: eight genera; (3) Chromi-nae: three genera; (4) Abudefdufinae: one genus; and (5) Pomacentridae: 16 genera (Cooper et al. 2009; Frederich et al. 2013). Three of these subfamilies, including seven genera and 24 endemic species, are found in the EP, distrib-uted from Monterey Bay, California, USA (Cooper 1863), in the North to the coast of Valdivia, Chile (Pequeño et al. 2005), and in the South (Fig. 1).

Hypotheses about the origin of the fauna in the Tropical Eastern Pacific suggest three main biogeographic sources as follows: (1) immigrants from the Indo-West Pacific fol-lowing long-distance dispersal before the formation of Isth-mus of Panama, (2) relict species derived from ancestral

species of the Atlantic, (3) local mixing of the biotas after the isolation of the eastern Pacific (EP) by environmental events (e.g., El Niño and La Niña), tectonic events, specia-tion and extinction, and (4) relatively recent evolution of endemic species in isolated or marginal environments in the EP (Glynn and Ault 2000; Cowman and Bellwood 2012).

The EP is biogeographically isolated by the Isthmus of Panama and the eastern Pacific barrier (Fig. 1). The grad-ual rise of the Isthmus of Panama marks the final closure between the Atlantic and EP around ~3–6 My (Duque-Caro 1990; Coates and Obando 1996; Glynn and Ault 2000; Bellwood and Wainwright 2002; Steeves et al. 2005; Bacon et al. 2015); this event leads to allopatric separation of spe-cies and, over time, to speciation.

The eastern Pacific barrier segregates the faunas of the EP and the Indo-West Pacific by 5000–8000 km of deep open ocean originate ~65 My ago (Ekman 1953; Dana 1975; Grigg and Hey 1992; Glynn and Ault 2000; Bell-wood and Wainwright 2002) (Fig. 1). The eastern Pacific barrier is really a strong filter rather than an absolute bar-rier and thus is not impassable as demonstrated by close related reef fishes species living in Indo-West Pacific and EP between which gene flow occurs (Lessios and Rob-ertson 2006; Cowman and Bellwood 2012). The Gulf of California barrier, dominated by the long peninsula of Baja California that segregates the faunas of the Pacific Ocean

Fig. 1 Geographic isolation of the Pomacentridae family in the eastern Pacific showing known occurrence records as black dots. Geological ages are indi-cated for the major geographic barriers and boxes identify island groups that are discussed in the text

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from the Gulf of California, began to form ~25 My ago, taking its present shape between 12 and 3.5 My (Holt et al. 2000; Riddle et al. 2000; Bernardi et al. 2003; Robertson and Cramer 2009; Castillo-Páez et al. 2014).

Biogeographic analyses showed that patterns of pro-vincialism in Tropical Eastern Pacific differ by taxonomic group (Ekman 1953; Briggs 1974; Boschi 2000; Hastings 2000; Glynn and Ault 2000; Robertson and Cramer 2009; Kulbicki et al. 2013). The most commonly used classifica-tion is from Robertson and Cramer (2009) in which they recognized three provinces based on reef and shore fishes: the Panamic and Cortez provinces along the mainland coast, and the Ocean islands province covering the offshore islands of the Tropical Eastern Pacific.

Habitat, food availability, ocean temperature and produc-tivity strongly influence the distribution of marine organ-isms (Grove et al. 1986). Pomacentrids species present a wide range of habitat preferences. In the EP, damselfishes are associated with coral and rocky reefs, rocky shores and kelp forests; shallow tropical or subtropical waters, main-land shores and islands (Clarke 1971; Grove et al. 1986; Robertson and Allen 2015); the maximum depth at which they have been recorded is 150 m (Greenfield and Woods 1980).

In this study, the geographic distribution of pomacentrid species within the EP was analyzed to elucidate the provin-ciality and the history of their radiation. The questions to be answered are: (1) which are the biogeographic provinces of damselfishes in the eastern Pacific, (2) where was the center of origin of the damselfishes of the eastern Pacific and (3) how has the center of origin shaped the current bio-diversity patterns of Pomacentridae?

Materials and methods

Distribution data

A matrix of geographic occurrences of the 24 pomacen-trid species from the EP was constructed based on the published literature (Allen 1991; Aguilar-Medrano et al. 2011; 2013; Robertson and Allen 2015). To geographically segregate the EP, we use the 14 Tropical Eastern Pacific regions proposed by Glynn and Ault (2000) based on coral reef distribution: (1) GOC, Gulf of California; (2) REV, Revillagigedo islands; (3) MXM, Mexican Province; (4) CLP, Clipperton island; (5) GUA, Guatemala; (6) SAL, El Salvador; (7) NIC, Nicaragua; (8) COC, Cocos island; (9) CRC, Costa Rica; (10) GAL, Galapagos islands; (11) PAN, Panama; (12) MAL, Malpelo island; (13) COL, Colombia; and (14) ECD, Ecuador, and three extra regions were added to cover all the damselfish distribution: (15) CP, California Province; (16) PRU, Peru; and (17) CHL, Chile (Table 1).

Size

The size of the 24 damselfish species in the EP was obtained from the literature (Allen 1991; Aguilar-Medrano et al. 2011; 2013; Table 1). The size of the species was calculated per provinces, and a MANOVA was performed using provinces as grouping factor. Finally, the relation between size and number of species per province was tested by regression.

Biogeography

The biogeographic similarity between areas within the EP was analyzed based on species occurrence data (Table 1) using two main approaches: cluster analyses and parsi-mony analysis of endemism (PAE). Three linkage methods of cluster analysis were used: (a) Jaccard similarity and (b) Bray–Curtis similarity, neither of which treat absences as evidence of similarity between groups and both of which use the average linkage method to compare the aver-age similarity values of all segment pairs within a cluster (Clarke 1993; Kosman and Leonard 2005; Robertson and Cramer 2009), and (c) Ward’s method, which is a clustering algorithm that optimizes based on within-group variance rather than raw distance (Ward 1963; Sneath and Sokal 1973; Kuiper and Fisher 1975; Mojena 1977; Glynn and Ault 2000; Goswami and Polly 2010). For all methods, the cophenetic correlation coefficient was used as measure of the goodness of fit of the dendrogram to the original data (Sokal and Rohlf 1962). All cluster analyses were com-puted with the statistical package PAST, version 3.0 (Ham-mer et al. 2001).

PAE is a parsimony-based tree algorithm that builds area cladograms from distribution data and is used to study historical relationships between areas and the evolu-tion of endemics (Rosen 1988; Cracraft 1991, 1994; Mor-rone and Crisci 1995; De Grave 2001), in which sympa-try may indicate a shared biological history (Morrone and Crisci 1995; Rosen 1988; Huang et al. 2010). PAE is one of the most widely used methods for describing biogeo-graphic patterns using presence/absence characters (Agui-lar–Aguilar et al. 2003; Riddle and Hafner 2006; Agui-lar–Aguilar et al. 2005; Contreras-Medina et al., 2007; Casagranda et al.2012; Mavrodiev et al. 2012; Szumik et al. 2012) in spite of the criticism of hierarchical meth-ods (Aagesen et al. 2009; Arias et al. 2010; Casagranda and Grosso 2013). Biogeographic analysis was carried out with TNT version 1.1 (Goloboff et al. 2003), which cal-culates all possible most parsimonious trees, a maximum of 100 trees saved per replicate, with 100 random addition replicates, using tree bisection and reconnection (TBR) as search strategy. All characters were treated as disarranged, and no weighting procedure was performed. Bootstrap

2294 Mar Biol (2015) 162:2291–2303

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Tabl

e 1

Geo

grap

hic

dist

ribu

tion

of th

e Po

mac

entr

idae

fam

ily in

the

east

ern

Paci

fic

0 in

dica

tes

abse

nce

and

1 pr

esen

ce

Loc

aliti

es c

odes

: RE

V R

evill

agig

edo

Isla

nds,

CL

P C

lippe

rton

Isl

and,

CO

C C

ocos

Isl

and,

MA

L M

alpe

lo I

slan

d, G

AL

Gal

apag

os I

slan

ds, C

P C

alif

orni

a pr

ovin

ce, G

OC

Gul

f of

Cal

ifor

nia,

MX

M

Mex

ican

pro

vinc

e, G

UA

Gua

tem

ala,

SA

L E

l Sal

vado

r, N

IC N

icar

agua

, CR

C C

osta

Ric

a, P

AN

Pan

ama,

CO

L C

olom

bia,

EC

D E

cuad

or, P

RU

Per

u, C

HL

Chi

le

n nu

mbe

r of

spe

cim

ens,

SL

A a

vera

ge s

tand

ard

leng

th o

f th

e fis

hes

used

in th

is s

tudy

, SL

B m

axim

um s

tand

ard

leng

th r

epor

ted

by A

llen

(199

1)

Spec

ies

nSL

A (

cm)

SL B

(cm

)L

ocal

ities

Tota

l cov

er

RE

VC

LP

CO

CM

AL

GA

LC

PG

OC

MX

MG

UA

SAL

NIC

CR

CPA

NC

OL

EC

DPR

UC

HL

Abu

defd

uf c

onco

lor

713

190

01

11

00

00

11

11

11

10

10

Abu

defd

uf d

ecli

vifr

ons

713

181

00

00

01

11

11

10

00

00

7

Abu

defd

uf tr

osch

elii

1013

231

11

11

11

11

11

11

11

10

16

Azu

rina

eup

alam

a5

1016

00

00

10

00

00

00

00

00

01

Azu

rina

hir

undo

813

171

00

00

00

00

00

00

00

00

1

Chr

omis

alt

a7

1015

11

11

10

11

00

00

00

00

07

Chr

omis

atr

ilob

ata

158

131

01

11

01

11

11

11

11

10

14

Chr

omis

cru

sma

1013

190

00

00

00

00

00

00

01

11

3

Chr

omis

inte

rcru

sma

516

280

00

00

00

00

00

00

01

11

3

Chr

omis

lim

baug

hi6

1112

10

00

00

11

00

00

00

00

03

Chr

omis

mer

idia

na12

1011

00

00

00

00

00

00

00

00

11

Chr

omis

pun

ctip

inni

s11

1925

00

00

01

00

00

00

00

00

01

Hyp

sypo

ps r

ubic

undu

s12

2036

00

00

01

10

00

00

00

00

02

Mic

rosp

atho

don

bair

dii

921

311

01

11

01

11

11

11

11

00

13

Mic

rosp

atho

don

dors

alis

2018

311

01

11

01

11

11

11

11

00

13

Nex

ilos

us la

tifr

ons

722

300

00

11

00

00

00

00

01

11

5

Steg

aste

s ac

apul

coen

sis

1512

180

01

11

01

11

11

11

11

10

13

Steg

aste

s ar

cifr

ons

1011

160

01

11

00

00

00

10

10

00

5

Steg

aste

s ba

ldw

ini

38

130

10

00

00

00

00

00

00

00

1

Steg

aste

s be

ebei

611

170

01

11

00

00

00

01

00

00

4

Steg

aste

s fla

vila

tus

1511

151

01

01

01

11

11

11

11

10

13

Steg

aste

s le

ucor

us12

1217

10

00

01

11

00

00

00

00

04

Steg

aste

s re

ctif

raen

um10

1013

10

00

00

11

00

00

00

00

03

Steg

aste

s re

dem

ptus

1012

151

00

00

01

00

00

00

00

00

2

Tota

l–

––

123

1010

124

1311

78

89

88

108

4

2295Mar Biol (2015) 162:2291–2303

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was conducted with 1000 replicates. Consistency index (CI), retention index (RI) and bootstrap replicate values were used as measure of goodness of fit of the area trees to the data. As recommended for PAE analyses, our over-all analysis was rooted with a hypothetical biogeographic ancestor of all zeros (absence; Morrone and Crisci 1995). To further test the biogeographic relationship between the EP damselfish with the Indo-West Pacific and Atlantic, we used two additional rooting relationships: (a) the relation-ship with the Atlantic using Panama as the root and (b) the relationship with the Indo-West Pacific using Galapagos Islands as the root.

Results

Pomacentridae provinciality in the eastern Pacific

All cluster analyses produced dendrograms with six main groups (Fig. 2): (1) the outlying localities in the extreme North (CP), South (CHL) and West (CLP); (2) oceanic islands and mainland Mexico (MXM, GOC, REV); (3) the southern localities (ECD and PRU); (4) southern Central America (PAN, CRC, COL): (5) Central America (GUA, SAL, NIC); and (6) EP equatorial islands (GAL, COC, MAL). However, using Jaccard and Bray–Curtis similar-ity, PAN is always basal to the central localities (GUA, SAL, NIC, CRC, COL). The cophenetic correlation coef-ficient was higher using Jaccard and Bray–Curtis similarity (0.951).

The PAE results were highly similar regardless of root-ing factor. Using GAL, we found seven most parsimonious trees, ten using PAN and 11 using the hypothetical root. The shortest trees rooted with both GAL and the hypo-thetical ancestor were 41 steps long, 40 using PAN as the root. The ensemble consistency index (CI) using GAL and the hypothetical root is 0.61, and 0.62 using PAN. The trees rooted with the hypothetical root yielded the highest ensemble retention index (RI): 0.75, while GAL yielded the lowest: 0.71 and PAN was intermediate at 0.73. Two clusters were conserved in all three analyses: (1) North (GUA, MXM, GOC, REV), which give the highest boot-strap values using PAN as rooting factor; and (2) EP equa-torial islands (GAL, COC, MAL), whose highest bootstrap values were with the hypothetical root (Fig. 3).

Based on the combined results (cluster and PAE), we recognize six provinces for damselfishes of the east-ern Pacific. (1) EPEI: EP equatorial islands (GAL, MAL, COC) recovered in all analyses (clustering and PAE). (2) N: North (GUA, MXM, GOC, REV) recovered in all analyses (clustering and PAE); the inclusion of GUA in this cluster is supported by all PAE analyses. (3) Center (SAL, NIC, PAN, CRC, COL), which is recovered in all the cluster analyses, but which is not recovered as a group in the PAE consensuses trees shows the central localities as non-group to any cluster. Cluster analyses recognize the southern localities as one subgroup (ECD, PRU) and extreme localities as another (CHL, CP, CLP), while PAE analyses using GAL and PAN as rooting factors lumped the two subgroups into one (ECD, PRU, CHL, CP, CLP).

Fig. 2 Cluster of the localities of distribution of the damselfishes in the eastern Pacific using three linkage methods: Ward, Bray–Curtis and Jaccard. Localities: GOC, Gulf of California; REV, Revillagigedo islands; MXM, Mexican Province; CLP, Clipperton island; GUA, Guatemala; SAL, El Salvador; NIC, Nicaragua; COC, Cocos island;

CRC, Costa Rica; GAL, Galapagos islands; PAN, Panama; MAL, Malpelo island; COL, Colombia; ECD, Ecuador; CP, California Prov-ince; PRU, Peru; CHL, Chile. Coph. corr.: cophenetic correlation coefficient

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(4) South (ECD, PRU, CHL), including CHL, and extreme localities. (5) Clipperton. (6) California Province (Table 2). Provinces 4, 5 and 6 are geographically coherent, and all three were recovered in the PAE tree rooted with the hypo-thetical ancestral area. A map showing the six provinces for damselfishes of the eastern Pacific, with additional infor-mation about temperature (Levitus and Boyer 1994), major sand gaps (Robertson and Cramer 2009) and productivity (chlorophyll a concentrations; Capone and Hutchins 2013), was used to visualize biogeographic patterns of the eastern Pacific (Fig. 4).

Patterns of distribution

The geographic distribution of damselfishes in the EP cov-ers a large area, from Monterey Bay, California, USA (36° 36′ 22″N, 121° 52′ 13″W; Cooper 1863), in the North to the coast of Valdivia, Chile (39° 51′ 12″S, 73° 23′ 56″W; Pequeño et al. 2005), and in the South, approximately 9860 km longitudinally (Figs. 1, 5). None of the 24 species

of damselfish found in the EP are found in any other ocean; thus, the endemism in the EP at the species level is 100 % and close to 50 % at the generic level, with three endemic genera: Azurina, Nexilosus and Hypsypops. The gen-era with the largest distribution are Chromis (100 % of the sites), Abudefduf, Stegastes (94.12 % of the sites) and Microspathodon (76.47 % of the sites). The species that are most widely distributed in the EP are A. troschelii (94.12 % of the sites), Ch. atrilobata (88.24 % of the sites), M. bair-dii, M. dorsalis, S. acapulcoensis and S. flavilatus (76.47 % of the sites). Ten species have restricted distributions (i.e., species that occur in less than 18 % of the sites). We cat-egorized these species into two progressively restricted groups: (1) endemic species: species found in two or three localities: Ecuador, Peru and Chile, Ch. crusma and Ch. intercrusma; Revillagigedo, Gulf of California and Mexi-can Province, Ch. limbaughi and S. rectifraenum; Gulf of California and California Province, H. rubicundus; Gulf of California and Revillagigedo islands, S. redemptus, and (2) microendemic species: those species present at only

Fig. 3 Parsimony analysis of endemicity of Pomacentridae family in the eastern Pacific. a Tree using a constructed root, b tree using Panama as rooting factor, c tree using Galapagos as rooting factor, d, e, f consensus trees of a, b and c. Numbers in the branches of a, b and c: bootstrap values. Numbers in the branches of d, e and f: branch length. GOC, Gulf of California; REV, Revillagigedo islands; MXM,

Mexican Province; CLP, Clipperton island; GUA, Guatemala; SAL, El Salvador; NIC, Nicaragua; COC, Cocos island; CRC, Costa Rica; GAL, Galapagos islands; PAN, Panama; MAL, Malpelo island; COL, Colombia; ECD, Ecuador; CP, California Province; PRU, Peru; CHL, Chile

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one locality: California Province, Ch. punctipinnis; Revil-lagigedo islands, A. hirundo; Clipperton, S. baldwini; and Galapagos, A. eupalama. The species with restricted distri-butions are principally found in islands or at the extremes of the Pomacentridae distribution (Fig. 5).

Considering species richness at the locality level, the islands with the highest number of species are: Galapa-gos, Revillagigedo (12 species each), Cocos and Malpelo (10 species each). The mainland coastal localities with the highest number of species are: The Gulf of California (13 species), Mexican Province (11 species) and Ecuador (10 species) (Fig. 5).

Size variation

The mean standard length for damselfishes from the EP is 13.39 cm; the species with the longest mean are N. lati-frons (mean 22.40 cm) and M. bairdi (mean 21.43 cm), while species with the smallest mean are S. baldwini (mean 7.79 cm) and Ch. atrilobata (mean 8.13 cm; Table 1).

Using provinces as grouping factor, the largest damself-ish are found in CP (mean 15.93 cm; max 19.76 cm; min 11.50 cm; n = 49 organisms) and South (mean 15.36 cm; max 22.40 cm; min 10.24 cm; n = 140 organisms); the mean values are registered for Center (mean 13.57 cm; max 21.43 cm; min 8.13 cm; n = 128 organisms), North (mean 13.10 cm; max 21.43 cm; min 8.13 cm; n = 174 organisms)

and EPEI (mean 13.73 cm; max 22.40 cm; min 8.13 cm; n = 142 organisms), while CLP presents the lowest val-ues (mean 10.41 cm; max 13.17 cm; min 7.79 cm; n = 24 organisms). The MANOVA of size shows significant dif-ferences between provinces (F5–651 = 3.82; p < 0.002), specially between three groups: (1) CLP, (2) CP and (3) S, N, C, EPEI. Number of species per province show no sig-nificant relation to size (r2 = −0.09; p = 0.08); this result could be related to the fact that areas with higher number of species present the biggest and smallest species due to a wider range of sizes, while the areas with few number of species present the intermedium values (see Table 2).

Discussion

One goal of biodiversity sciences is to understand the his-torical phases that a group in developing its present pat-terns of diversity. Reef fish are an important group of more than 5000 species (Bellwood et al. 2010), and damself-ishes are the third largest reef fish group, with 394 species (Eschmeyer 2015). Most damselfishes inhabit the central Indo-Australian Archipelago (60 %), and the EP damself-ish community is thus smaller than the communities in any other sea (Atlantic, Indian Ocean, Central Pacific and Indo-Australian Archipelago; Cowman and Bellwood 2012). However, the biogeographic characteristics of the

Table 2 Localities, provinces and variables

Abrev abbreviation

Localities Abrev. Province Abrev. Size (cm) Spp. number

Guatemala GUA North N Mean 13.1 14

Mexican Province MXM Max. 21.43

Gulf of California GOC Min. 8.13

Revillagigedo islands REV

El Salvador SAL Center C Mean 13.57 10

Nicaragua NIC Max. 21.43

Panama PAN Min. 8.13

Costa Rica CRC

Colombia COL

Galapagos islands GAL Eastern Pacific EPEI Mean 13.73 12

Malpelo island MAL Equatorial islands Max. 22.4

Cocos island COC Min. 8.13

Ecuador ECD South S Mean 15.07 10

Peru PRU Max. 22.4

Chile CHL Min. 8.13

California Province CP California CP Mean 15.93 4

Province Max. 19.76

Min. 11.5

Clipperton CLP Clipperton CLP Mean 10.41 3

Max. 13.17

Min. 7.79

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EP community make it especially interesting due to: (1) endemicity; three of the seven genera (Azurina, Hypsypops and Nexilosus) and 100 % of the species of the area are

endemic and (2) physical conditions; most of the eastern Pacific environments are influenced by temperate currents, which favor rocky reefs or kelp forest over coral reefs.

Fig. 4 Biogeographic provinces of damselfishes of the eastern Pacific indicating major eco-logical barriers as: superficial water temperature (Levitus and Boyer, 1994), sand gaps (Rob-ertson and Cramer, 2009) and areas of maximum concentra-tion of chlorophyll a (Capone and Hutchins, 2013)

Fig. 5 Connection web for the six biogeographic provinces of the Pomacentridae family in the eastern Pacific. EPEI, EP equatorial islands; S, South; CP, California Province; CLP, Clipperton island; C, center; N, North. a Diversity. Numbers in parentheses indicate the number of species in each region. Colors represent genera, and the size of each slice is proportional to the number of species. b Endemicity and interconnec-tions. Numbers report the shared species between provinces. Colors represent genera and the size of each slice is proportional to the number of endemic spe-cies per genus

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Thus, it is of special interest to understand the patterns of diversification of damselfish in the eastern Pacific, which might be a key to understanding the worldwide radiation of this fish family.

Diversification in the eastern Pacific

The number of provinces in the Tropical Eastern Pacific has been studied intensively, but with little resolution as the classification depends strongly on which group is being analyzed, suggesting that the ecology and biogeography of the eastern Pacific are not governed by overarching fac-tors that apply to all taxa. Each group may respond to the complex of eastern Pacific factors differently. Indeed, the factors that are important in the distribution of the reef fish communities differ from analysis to analysis. For example, the two stretches of sand and mud shorelines, the Sinaloan Gap (370 km of shoreline) and the Central American Gap (~1000 km of shoreline; Robertson and Cramer 2009), were identified as important factors in the provincial clas-sifications by Ekman (1953), Walker (1960) and Hastings (2000), but not in the classifications of Briggs (1974), Boschi (2000), Spalding et al. (2007), Robertson and Cramer (2009) or our analyses (Fig. 4). Water temperature fluctuates considerably over time and space in the EP. The latitudinal range from equatorial to temperate regions varies greatly due to climate events such as El Niño and La Niña that change the range of temperatures, the spatial range and the speeds of the ocean currents from year to year, and the seasonal upwelling systems scattered throughout the region (Glynn and Ault 2000; Robertson and Cramer 2009). It appears that the upwelling of California and Ecuador may be important in defining the extreme North and South dis-tribution of damselfishes, probably due to food availability (Fig. 4).

The EP equatorial islands (GAL, COC, MAL) are influ-enced by three major ocean currents: the southern area of these islands receives the temperate Humboldt Current, the northern receives the moderately warm North Equato-rial Current and the Equatorial undercurrent causing a cold upwelling rich in nutrients near the western shores (Car-rasco 2000). The central localities (SAL, NIC, PAN, CRC, COL) are mainly affected by the Contra and North Equato-rial currents, with higher water temperatures than the EPEI. Our analyses show that the EPEI and the Central Province share nine species, of which six are widely distributed in the EP and one is endemic to the EPEI. The Central Prov-ince has no endemic species. The Central Province appears to have fewer barriers to dispersal due to its environment conditions as similar temperature in the whole area as well as no physical barriers and thus functions as an area of overlap or a corridor from Galapagos to the Gulf of Cali-fornia, the two areas with the largest number of species.

At one time, damselfishes had colonized the central area (EPEI and Central) by immigration from the Indo-West Pacific; relict species derivate from the ancestral connec-tion with the Atlantic and local mixing (Glynn and Ault 2000; Cowman and Bellwood 2012). They then spread both to the North (REV, GUA, MXM, GOC) and South (ECD, PRU, CHL). Both these areas have different physical con-ditions that impact distributions. The North and the South have fewer coral reefs and are dominated by rocky reefs and kelp forest (Steneck et al. 2002). Both regions are influ-enced by temperate currents: the California Current in the North and the Humboldt Current in the South. And in these regions occur some of the most important upwelling areas of the eastern Pacific (Capone and Hutchins 2013; Fig. 4). The conditions of these areas (especially CP, PRU, CHL) are thus highly different from the Central Province, and diversification in these latitudinally extreme areas is limited (CP and CHL host only four species each). Damselfish spe-cies inhabiting these localities are mainly endemic, three Chromis species in the South (ECD, PRU, CHL) and six species of Chromis, Hypsypops, Azurina and two Stegastes in the North (REV, GOC, MXM, GUA).

Kelp forests found in shallow rocky coasts and cold temperate waters are generally diverse and productive eco-systems (Mann 1973; Stephens et al. 2006). However, few damselfish populations persist in these environments. In the North, species as Hypsypops rubicundus and Chromis punc-tipinnis are two well-known kelp forest damselfish, while in the South there is Ch. crusma. One important adaptation of damselfishes to these environments was increase in body size. Bergmann’s rule (Bergmann 1847) posits that the body size of an animal should be larger in colder climates (poles, higher latitudes). This rule holds for damselfishes from the EP. One of the classic explanations of the Bergmann rule in ectotherms is that at relatively lower temperatures ecto-therms typically mature later and thus at larger sizes than conspecifics at higher temperatures (Ray 1960; Atkinson 1994; Sibly and Atkinson 1994). In this particular study, the size-temperature relationship also could be related to the increased swimming cost on temperate environments, which may be offset by higher energy reserves afforded by large body fishes. Potentially allowing damselfishes in these demanding habitats to swim for longer periods of time.

The Gulf of California, which is part of the North prov-ince, presents favorable conditions for the development of marine life and is home to the highest number of dam-selfishes in the EP (13 species). The Gulf of California has been recognized as one of the most diverse and unique ecosystems on the world, comprising a macrofauna of approximately 5969 species, 4854 invertebrates and 1115 vertebrates from where 891 are fishes and from these 77 are endemic (Brusca et al. 2005; Lluch-Cota et al. 2007). This diversity may be related to protection from heavy swell

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provided by the semi-enclosed area, to the highly complex structure of habitats (Munday and Jones 1998; Robertson and Cramer 2009), to its high productivity (Capone and Hutchins 2013), and to the grading of temperature and the habitat heterogeneity from its subtropical southern mouth, which support coral reefs, to its temperate northern head with rocky reefs (Robertson and Cramer 2009).

Clipperton Island has the most remote reefs of the EP, located 1.110 km southwest of the Mexican coast and 950 km South of Revillagigedo Islands. Clipperton has the largest coral reef in the EP and is strongly influenced by the warm waters of the North Equatorial Current (Robertson and Allen 1996). Clipperton shares one wide distributed species (Abudefduf troschelii) with most other EP locali-ties, one species with the North province (Chromis alta), and has one endemic species (Stegastes baldwini). Revil-lagigedo Islands, the closest habitat to Clipperton, host four of the eight species of the genus Stegastes, and the occurrence of S. baldwini at Clipperton may be the result of peripheral speciation from Revillagigedo islands; how-ever, to prove this point a good phylogeny is needed. Also, while Clipperton Island is a tropical area with high coral cover whose conditions could support many more species, the low number of species there could be the result of (1) habitat/food availability, since the island is small (6 km2, Robertson and Allen 1996). Habitat and food availability have shown to be important variables to explaining recent shifts or contractions/expansion in the ranges of distribu-tion (Fenberg et al. 2014; McCabe and Olson 2015), and (2) geographic distance between the island and the main-land, which constitutes a potential barrier to dispersal and gene flow (Muss et al. 2001).

While diversity in islands is limited by the distance to the mainland and the area of the island, as was observed in the Clipperton fauna, in continental areas ocean tempera-ture can often be the limiting factor, as observed in Chile and California Province, where temperate ocean currents create environments where only a few damselfish, most of them endemic, can survive and persist. In these temper-ate environments damselfish tend to be larger and stouter, characters that allow them to amass energy reserves to deal with the low temperatures.

Center of origin versus center of richness

It has been hypothesized that the centers of origin and speciation present general characteristics such as: (1) high diversity, (2) closeness of phylogenetic relationships among taxa, (3) sympatric speciation, and (4) phylogeneti-cally young species (McManus 1985; Briggs 1999; 2003; Mora et al. 2003). This model of centers of origin thus sup-poses that they are also centers of richness. Previous bio-geographic analyses of the eastern Pacific have found, as

did ours, two centers of species richness, one subtropical and the other equatorial (Glynn and Ault 2000; Robertson and Cramer 2009). In our study, the subtropical center of species richness is the Gulf of California, while the equa-torial center of species richness is Galapagos Islands. In the North Province, the Gulf of California has the highest diversity of damselfish species (13 of 24 species), of which six are widely distributed species (present in 13–16 of the 17 total localities) and three species are endemic (defined here as species present in two to three of the 17 localities), while the equatorial center of species richness, Galapagos Islands, has 12 species, six are widely distributed species and one microendemic species (defined here as species pre-sent in only one locality). Both centers of richness have (1) high diversity, (2) closeness of phylogenetic relationships among taxa, (3) sympatric speciation and (4) phylogeneti-cally young species.

However, our analyses provide support for the Central Province as the center of origin of eastern Pacific poma-centrids based on bootstrap values, even though it is not a center of richness. The Central Province (SAL, NIC, CRC, PAN, COL) has medium richness made up of non-endemic species (Fig. 5). Richness and endemicity increase to the North (GUA, REV, MXM, GOC) and in the EP equatorial islands (GAL, COC, MAL). However, the central locali-ties share the largest number of species with EP equatorial islands, North and South (Fig. 5). The Equatorial Contra Current favors the dispersion of larvae from the Central Province and EP equatorial island to the North through the North Equatorial Current and the South through the South Equatorial Current (Grigg and Hey 1992; Lessios and Robertson 2006; Robertson and Cramer 2009; Wood et al. 2014). The Central Province also is home to the four genera with the widest distribution (Abudefduf, Chromis, Micro-spathodon, Stegastes), all of which have closely related species in the west Atlantic (ATL), including A. troschelii (EP) and A. saxatilis (ATL), which, based on holoenzymes, diverged only 5.8 My (Gorman and Kim 1977), Ch. atri-lobata (EP) and Ch. multilineata (ATL), which, using hypervariable portion of the mitochondrial control region (D-loop), diverged 0.93–3.26 My (Domingues et al. 2005), and M. dorsalis (EP) and M. chrysurus (ATL) which, using nuclear and mitochondrial gene fragments, diverged approximately 6–7 My (Frederich et al. 2013), all consist-ent with the final closure of the Isthmus of Panama around 3–6 My (Duque-Caro 1990; Coates and Obando 1996; Glynn and Ault 2000; Bellwood and Wainwright 2002; Steeves et al. 2005; Bacon et al. 2015).

In summary, our results reveal the radiation of Poma-centridae in the eastern Pacific to be a dynamic disper-sion system, whose history can be segregated into three main steps: (1) mixture and speciation of species with close affinity to west Atlantic ancestral stocks in the

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Central Province, (2) dispersion due to favorable condi-tions of the Gulf of California and Galapagos islands and (3) the more complex and perhaps long, gradual dispersal and radiation to temperate areas and isolated or marginal environments.

Acknowledgments Consejo Nacional de Ciencia y Tecnología (CONACYT, Mexico) funded the research of R. Aguilar-Medrano. The manuscript benefited from comments by E. Balart Páez, X. Moreno Sánchez, M. Taylor and one anonymous reviewer.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of interest.

Ethical standard This study did not use organisms.

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