Signals of Adaptive Genetic Variation in BC’s Nearshore Rockfish: Implications

8/14/2019 Signals of Adaptive Genetic Variation in BC’s Nearshore Rockfish: Implications

http://slidepdf.com/reader/full/signals-of-adaptive-genetic-variation-in-bcs-nearshore-rockfish-implications 1/22

Signals of adaptive genetic variation in BC’s nearshorerockfish:

implications for population connectivityMatthew Siegle

IntroductionDegradation of the world’s oceans, including fishery

overexploitation (Botsford et al. 1997), loss of marine biodiversity

(Worm et al. 2006), increases in eutrophication (Rabalais et al. 2009),

and the effects of climate change (Lotze et al. 2006) have forced

scientists and resource managers to rethink current approaches to the

maintenance of marine ecosystems (Lubchenco et al. 2003, Hughes et

al. 2005). Changes from single species to ecosystem level

management methods have provided insight into the usefulness of

marine reserves for the preservation of marine ecosystem services

(Agardy 1994, Halpern 2003, Lubchenco et al. 2003). Reserves are

able to mitigate human pressures through a variety of measures,

including the protection of vulnerable life stages, mating and nursery

grounds, providing spatial refuge for harvested species and exporting

individuals into depleted areas. However, Allison et al. (1998) warn

against viewing marine reserves as a magic bullet, and highlight thatcommunities residing in marine reserves are highly influenced by the

continuous flow of water through reserve areas, and thus susceptible

to threats originating outside reserve boundaries (e.g. pollution).

Nevertheless, marine reserves remain a powerful tool in conservation

and management.

The empirical data showing the positive role reserves have in

increasing biodiversity, abundances and densities within their

boundaries is reasonably well established (Castilla and Bustamante

1989, Roberts 1995, Halpern and Warner 2002, Halpern 2003). What is

less clear, however, is the role reserves play in exporting these

benefits to outside areas (Agardy 1994, Palumbi 2003). Understanding

how reserves function in the greater ecosystem beyond their



boundaries is crucial for the integration of reserves into ecosystem and

regional scales of management. For example, the success of fisheries

reserves depends on their ability to export individuals into areas

targeted for exploitation (DeMartini 1993, Palumbi 2003).

Understanding the export of individuals is also crucial for the

development of reserve networks, where local replenishment depends

on upstream source populations. Thus, understanding how reserves

function at regional scales necessitates identifying source and sink

populations and the mechanisms through which populations are

connected (Levin 2006).

Many demersal marine fishes exhibit a two-phase life cycle,

including a dispersive larval phase and a sedentary adult phase. Larval

development occurs in the water column before individuals recruit to

adult habitat, and can last on the order of weeks to several months.

During this larval phase, individuals have the potential to be

transported hundreds of kilometers via water currents. This capacity

for long distance larval dispersal coupled with a (relative) lack of

physical barriers in the ocean has led to the notion that marine

populations are subject to demographic processes from geographicallydistant populations (Warner and Cowen 2002).

This “open population” model predicts the widespread

homogenization of regional population structure (Palumbi 1994) and is

corroborated by many earlier genetic surveys of marine fishes, which

found a lack of genetic differentiation across extensive geographic

areas (Ward et al. 1994). While gene flow may dampen the ability of

local populations to adapt to local conditions (Slatkin 1973), marine

fishes occupy extensive geographical ranges and diverse

environmental conditions (Hemmer-Hansen et al. 2007). It is likely that

local selection can override the homogenizing effects of gene flow,

revealing finer scale patterns of local adaptation and providing insight

into population substructure (Conover et al. 2006). Additionally, weak



estimates of structure that are spatially and temporally stable and are

correlated with environmental factors, bolsters the argument for weak,

yet biologically relevant genetic structuring (Hauser and Carvalho

2008).

The Stock Concept and Neutral Population Structure

Many genetic studies of marine fishes utilize neutral genetic

variation to describe spatial population structure. Neutral markers

escape the confounding effects natural selection imposes on allele

frequencies and allows researchers to estimate demographic

parameters without needing to account for the biases associated with

environmental influences (Conover et al. 2006). Studies of spatial

population structure in marine fishes are often undertaken for the

purpose of delineating individual stocks. Many variations of the stock

concept can be found in the literature (Carvalho and Hauser 1994), but

generally, a stock refers to a group of individuals that share similar

demographic and genetic trajectories (Waples 1998). The stock

concept is especially popular with fishery managers, who treat

individual stocks as independent populations and can target a stock for

exploitation without worrying about the impact on other stocks. Theusefulness of the stock concept, however, depends on our ability to

correctly differentiate two putative stocks from a set of biological traits

(morphological, genetic, etc.), and typically utilizes a suite of statistical

tests to do so (Waples 1998). However, it is critical that we realize the

potential disconnect between statistical and biological significance. A

null statistical result (indicating no differentiation between areas)

doesn’t immediately indicate a single panmictic stock, and treatment

of such could lead to the overexploitation of certain areas. Conversely,

provided there is enough data, it is probable that statistically

significant differences will be found (indicating two stocks), which may

not have any biological relevance. This can lead to the underutilization

of a resource at a societal cost (Waples 1998). Thus, it is critical that



we understand the limitations of our data and integrate the potential

disconnect between statistical and biologically significance into our

interpretations of geographic population differentiation.

The high rates of gene flow and low levels of differentiation

observed in marine fishes complicate the use of the stock concept.

Neutral genetic variation is most often estimated using Wright’s F-

statistics (Wright 1931), of which FST is the most pertinent to spatial

studies of gene flow (Whitlock and McCauley 1999). FST is a measure of

total genetic variation between populations, and can be used globally,

comparing the amount of genetic variation in a subpopulation to the

total amount of genetic variation observed, or in pair-wise comparisons

that estimate differentiation between two populations. High FST values

indicate a high degree of differentiation and low FST values suggest

minimal differentiation. However, interpreting the biological meaning

of low FST values are complicated by a number of factors.

FST is a cumulative estimate of gene flow measured over

evolutionary time scales, and it is often difficult to tease apart

historical processes from contemporary patterns of gene flow. For

example, genetic surveys of recently diverged populations with littlecontemporary gene flow may still exhibit low FST values, as not enough

time has elapsed for genetic differences to accumulate between the

two populations. In this situation, historical levels of gene flow, not

contemporary (ecologically relevant) patterns dominate the FST

estimate. Moreover, as Waples (1998) pointed out, only a handful of

migrants per generation are required to homogenize allele frequencies.

Ecologically insignificant, rare dispersal events over evolutionary time

are sufficient to falsely indicate a pattern of consistent larval

exchange, which would indicate contemporary demographic

connectivity. Additionally, neutral gene flow can persist in the presence

of strong divergent selection. As only a handful of migrants are

sufficient to homogenize neutral allele frequencies, rare migrants



surviving despite being maladapted would mask the presence of strong

selection against the vast majority of migrants. Furthermore, slight

signals of differentiation are greatly complicated by the amount of

statistical noise inherent in surveys of marine fishes. Nonrandom

sampling and small sample sizes contribute to errors in FST estimates.

With increasing estimates of FST, the sampling error becomes less and

less relevant. However, with low estimates of FST, the sampling error

takes on greater importance and can be responsible for a greater

proportion of the raw FST observed (Waples 1998).

Careful consideration must be given when interpreting

population divergence under scenarios of low FST values. Statistical

limitations and the potential confounding influences of historical

processes on contemporary dynamics hamper our ability to extract

meaningful biological information from low FST estimates.

Understanding regional patterns of population structure and

connectivity and the dynamics between source and sink populations

are critical for both sustainable resource exploitation and conservation

initiatives. Fortunately, there are measures researchers can take to

maximize the information from genetic data. Waples (1998)recommends large sample sizes to reduce sampling bias and utilizing

many loci to reduce the variance of FST estimates across loci.

Additionally, sampling schemes that show temporally and spatially

stable patterns of population structure can bolster the argument for

biologically significant structure despite low statistical support.

Furthermore, Selkoe et al. (2008) advocate a multidisciplinary

approach to population structure and connectivity. They argue for the

integration of multiple data types, including recruitment time series

data, larval behavior studies and oceanographic modeling that can

augment genetic data difficult to interpret due to the problems

inherent with limited degrees of differentiation.

Local Adaptation and Connectivity in Marine Fishes



Local adaptation is the interaction between genotype and

environment that results in native individuals having a greater fitness

than their non-native counterparts. If there were no limitations on

adaptive divergence, we could expect individuals to be highly adapted

to their immediate surroundings on a fine spatial scale. However,

several factors limit the extent of local adaptation, including gene flow,

genetic drift, unpredictable temporal environmental instability, low

heritability of a trait, and trade-offs among traits (Conover et al. 2006).

The degree to which a group of individuals will be locally adapted

depends upon the strength of selection overriding the homogenizing

effect of these factors. For marine fishes, large effective populations

minimize the effects of drift and the high dispersal potential suggests

that gene flow is a major hindrance dampening the ability for local

adaptation to evolve. Thus, the strength of selection needs to be

sufficient to override the effects of gene flow. If divergent selection is

strong enough, dispersal will be severely restricted, and signals of

differential adaptation should be identifiable.

Investigating the geography of local adaptation in marine fishes

has important consequences for interpreting population structure,inferring connectivity between areas, and for understanding the

genetic diversity underlying phenotype. Signals of adaptive divergence

may correlate with weak signals of differentiation at neutral loci,

bolstering the argument for biologically significant structure.

Additionally, estimates of quantitative genetic variation (genetic

variation directly responsible for phenotypic variance) have been found

to occur on finer spatial scales than estimates of neutral genetic

variation (McKay and Latta 2002). Thus, if selection is strong enough,

signals of adaptive differentiation may resolve population structure on

a finer scale than neutral genetic structure and can be integrated with

environmental data to provide measures of population structure that

correlate with environmental heterogeneity.



Utilizing adaptive genetic variation to investigate population

structure also has implications for how we infer the degree of

connectivity between areas. More general notions of connectivity focus

on identifying independent larval sources contributing to recruitment in

a target area and the respective proportions of recruits originating

from the different source areas. However, measures of disperser

success are not addressed with traditional definitions of connectivity.

Thus, there is a potential disconnect between recruitment and

postsettlement survival. Hamilton et al. (2008) investigated this

scenario by studying the effects of different larval histories on

postsettlement survivorship in a population of Caribbean reef fish.

They found an asymmetrical pattern of postsettlement mortality. While

locally produced larvae constituted roughly 45% of the recruitment

pool, they composed only 23% of the total number of fish that survived

the first month after settlement. Thus, the fittest recruits, those with

the highest postsettlement survivorship rates, were dispersers from

offshore waters. The authors suggest that “realized connectivity”,

where the fitness and reproductive potential of the recruit are

considered, might be a more realistic metric of population connectivitythan simply identifying populations of origin and relative larval

contributions.

Mapping the geography of adaptive genetic variation provides

insight into the genetic diversity underlying phenotypic expression and

how this diversity is represented in heterogenous environments

(Hauser and Carvalho 2008). Variation in adaptive genetic diversity

may vary regionally. High levels of adaptive genetic diversity likely

entails a greater potential for populations to adapt, and a higher

likelihood of persistence in the face of changing environmental

pressures. Our ability to effectively manage fishery stocks over the

long term depends on our ability to predict how population

demographics may shift with environmental perturbations and



climatological changes. Identifying the genetic architecture underlying

population persistence amidst specific environmental pressures will

enable us to estimate how well populations may respond to

environmental changes or the potential for successful colonization

following local extirpations.

Rockfish and the Rockfish Conservation Areas

Rockfish (genus Sebastes) are a speciose group of marine fishes

that exhibit an impressive diversity of morphological and ecological

variation. Over 100 species from all over the world (~70 from

northeast Pacific, ~25 from northwest Pacific, seven from the Gulf of

California, four from the north Atlantic, and two in the southern

hemisphere) comprise the genus (Hyde and Vetter 2007). Rockfish

occur from shallow intertidal waters to depths well below 2,500

meters. They occupy all types of benthic and pelagic habitats,

including highly complex boulder and rock piles, sandy and muddy

bottoms and kelp forests (Love et al. 2002). Many species exhibit

extreme site fidelity and aggressively defend their home range, while

others form dense aggregations or schools. The benthic species are

often large, deep bodied and heavily armored with venomous spines.Pelagic schooling species are generally more streamlined and exhibit

reduced spination (Love et al. 2002).

This tremendous ecological variation highlights the integral role

rockfish have through out the nearshore ecosystems of North America.

However, the life history (slow growing, long lived, late to mature,

highly variable juvenile recruitment) of many rockfish species makes

them susceptible to overfishing (Parker et al. 2000, Love et al. 2002).

Overexploitation by commercial and recreational fisheries has led to

the decline of many previously abundant species (Lea et al. 1999) and

has prompted conservation concerns in the United States (Federal

Register 2008) and Canada. Bocaccio and canary rockfish (S.

paucispinis and S. pinniger ) are currently listed as threatened by



COSEWIC (Committee On the Status of Endangered Wildlife in Canada;

COSEWIC Status Reports 2002, 2007) and several more are under

review for protective status.

In response to the mounting conservation concerns surrounding

rockfish, Fisheries and Oceans Canada (DFO) recently implemented a

system of 164 marine proteted areas (MPAs), termed Rockfish

Conservation Areas (RCAs; Figure 1). Within RCAs, fishing activities

negatively impacting benthic rockfish (most notably: yelloweye,

quillback, copper, tiger and China (S.-ruberrimus, -maliger, -caurinus,

-nigrocinctus, and -nebulosus, respectively)) have been banned. The

RCA system is distributed along the entire British Columbia coast, and

represents one of the largest MPA systems in the world. However,

connectivity between RCA sites was not evaluated before or after RCAs

were established, and thus, the extent to which individual RCAs

function in concert as a network is unknown.

Functioning as a network is crucial for the overall success of the

RCA system. The ability of RCAs to augment depressed areas requires

that they maintain a reproductively healthy group of individuals. If the

degree of self-recruitment is low, this may depend on a consistentsupply of larvae from upstream areas. Thus, RCAs may be responsible

not only for exporting larvae into depressed areas, but also for the

maintenance of healthy breeding groups in downstream RCAs. An

understanding of regional connectivity, including the identification of

sources and sinks will ensure that RCAs are functioning not only to

augment depressed populations but also contribute to the

maintenance of the RCA network itself.

Project GoalsI am interested in identifying regions of the BC coast that may be

subject to varying selective pressures. Identifying areas of divergent

selection will elucidate potential barriers to dispersal and refine the

scales of connectivity along the BC coast. This has important



consequences for understanding the structuring of rockfish populations

and how the RCAs promote regional connectivity. I will be investigating

these processes in two species of nearshore rockfish: yelloweye (YE)

and quillback (QB), both of which are important in commercial and

recreational fisheries and are specifically targeted for protection by the

RCAs.

Background

DFO performed two population genetic/demographic studies on

YE and QB rockfish (Yamanaka et al. 2006a, Yamanaka et al. 2006b,

respectively). The findings of Yamanaka et al. (2006a) were consistent

with two distinct YE populations: an “inside” population (corresponding

to Management Areas 12 to 20, 28, and 29; Yamanaka and Lacko

2001), and an “outside” population (containing all fish not classified as

“inside”; (Figure 2). Sufficient genetic differentiation between the two

populations warranted a Designatable Unit (DU) status by COSEWIC for

both populations, the loss of either one of these DUs representing a

significant gap in the species’ historic range in Canada (COSEWIC

Status Report 2008). The “inside” DU was characterized by a reduced

heterozygosity (avg = 72.5% for outside, 62.7% for inside), smallereffective population size (2/3 that of outside DU) and a loss of rare

alleles.

Investigations by Yamanaka et al. (2006b) into QB rockfish

revealed no significant population structuring along the coast of BC.

Allele frequency distributions indicated that greater than 95.5% of

genetic variation occurred within sample locations and less than 0.5%

of genetic variation was attributable to differentiation between

samples. Additionally, estimates of effective population size for both

QB and YE were large, as expected for a widely distributed marine fish.

The two studies by Yamanaka et al. indicate that neutral gene

flow is extensive among QB and only slightly less so in YE. However,

the large region surveyed in these two studies encompasses several



environmental gradients, including salinity, depth, primary production,

varying ocean current patterns and a latitudinal cline. It is likely that

these environmental factors promote further population subdivision

than was provided by investigating neutral genetic structure.

Questions

Yelloweye

• Are there signatures of adaptive differentiation between“inside” and “outside” YE DUs?

• Do estimates of adaptive differentiation provide evidence forfurther substructure within each YE DU?

• Is adaptive differentiation correlated along any environmentalgradients?

Quillback

•

Do estimates of adaptive differentiation provide evidence forgenetic structure among coast-wide samples?o If so, is adaptive differentiation correlated along any

environmental gradients?Interspecific

• Does the degree of adaptive differentiation observed reflectthe varying levels of gene flow suggested in the Yamanaka etal. reports?

• If adaptive differentiation is found to occur along anyenvironmental gradients, do YE and QB rockfish share thesame pattern of differentiation?

Methods Sampling

Approximately 2500 YE individuals and 1500 QB individuals were

collected by DFO longline surveys from all over the BC coast (Figure

3a, b). Morphological and age data were collected in addition to

genetic tissue samples, and are included in the Yamanaka et al.

(2006a, b) reports.

Molecular Methods

I will utilize amplified fragment length polymorphisms (AFLPs)modified from Vos et al. (1995) to identify signatures of selection

across the genome of yelloweye and quillback rockfish. AFLPs utilize

restriction enzymes to cut the genome at known sequences. Primer

adapters (DNA sequences with 3’ overhangs complementary to the

single-strand 5’ overhangs left over from the restriction enzymes) are



ligated to the digested DNA. PCR primers are then added and bind

complementarily to the adapters. DNA sequences between restriction

sites are amplified via PCR and the resulting fragments are separated

by size. Each size fragment corresponds to a different restriction

fragment, and represents one locus. AFLP allows the rapid

amplification of a plethora of loci. PCR primer pairs include 3-4 variable

sites, and different combinations are used to amplify different loci. For

example, a primer with –AAC will bind to loci with the corresponding –

TTG sequence. Thus, utilizing 3 variable sites can amplify 46 different

loci (43 for each forward and reverse PCR primer).

Statistical Methods

The allelelic frequentist approach to identifying selection

generates neutral estimates of FST to locate outlier loci (those with FST

estimates outside the threshold values of neutrality). I will utilize the

hierearchical Bayesian approach in the Dfdist program of Beaumont

and Balding (2004). This program groups loci with higher than neutral

FST estimates as being subject to directional selection, and those with

lower than neutral FST estimates under balancing selection. However,

the ability to detect loci under balancing selection is generally low(Beaumont and Balding 2004). Fortunately, as the goal of this study is

to identify groups of fish under divergent selection, this limitation

becomes inconsequential.

AFLP data is scored on a dominant basis as present or absent,

therefore null allele frequencies will be estimated at each locus using

Zhivotovsky’s (1999) Bayesian approach. This allows the estimation of

FST at each locus. A neutral FST value will be calculated by removing

30% of the highest and lowest FST values estimated from the empirical

data (leaving a ‘trimmed’ FST value; Bonin et al. 2006, Gagnaire et al.

2009). A coalescent simulation approach is then used to generate a

mean FST from a distribution based on the ‘trimmed’ FST. An outlier

threshold is defined by establishing quantiles of simulated FSTs. Outlier



FSTs are identified as falling outside the neutral bounds. I will ignore

any FST values falling below the lower bound of neutrality due to the

difficulties of identifying balancing selection. Because I am

investigating adaptive differentiation in high gene flow species, and

predict that the discovery rate of outlier loci will be extremely low, I

will perform exploratory screens of many loci in representative groups

to identify outlier loci. Once candidate outlier loci have been observed

between groups, I will screen individuals from each of the respective

groups (Figure 4).

The respective groupings will represent:

(1) inside and outside yelloweye DUs

(2) local areas designated by the Yamanaka et al. reports (both YE andQB)(3) areas along environmental gradients (salinity, primary productivity,

depth and latitude)

Project SignificancePatterns of connectivity and the identification of dispersal

barriers drive the spatial scales at which we manage marine

populations. Variability in the postsettlement fitness of recruits from

different source populations has profound effects on regional

metapopulation dynamics. Investigating adaptive genetic

differentiation has the potential to further refine the scales at which we

infer population connectivity. Management decisions based on

incorrect models of connectivity can lead to overexploitation of a

resource. However, patterns of connectivity and estimates of

population structure from neutral loci are potentially subject to the

confounding influences of historical processes and are often difficult to

interpret due to low statistical support. The biological significance of

weak structure can be corroborated by additional data used in a

multidisciplinary approach, including additional genetic data that

highlights the potential role divergent selection has in structuring

populations. It is especially useful if signatures of local adaptation can



be correlated with variation along an environmental gradient, which

provides a direction for future, more detailed research.

The RCAs are one of the largest systems of marine protected

areas in the world. However, it is unclear how they function as a

network and serve as sources of larvae for exploited areas of the

coast. Previous work by DFO in YE and QB rockfish has found patterns

of limited population differentiation and extensive gene flow. However,

these estimates are based on neutral markers, and don’t reflect the

vast differences in environmental conditions found throughout coastal

BC. Thus, the potential for greater population structuring due to

environmental constraints is very likely. The success of the RCAs

depends not only upon their ability to export larvae into areas subject

to exploitation, but to ensure larvae are exported into areas they are

ecologically suited for. Incorporating measures of local adaptation will

help us understand how rockfish dispersal is limited by environmental

conditions and how well the RCA network promotes connectivity

amidst a dynamic and varying seascape.

Projected Timeline

December 2009-May 2010: Lab work/data collection June 2010-August 2010: Data analysis

September 2010-December 2010: Manuscript preparation/Thesis

defense

Projected Budget

(working on it)



Appendix

Figure 1: Rockfish Conservation Areas as of 2005.

Figure 2: YE DU classification; based on the findings of Yamanaka et al.(2006a). Shaded areas correspond to the “inside” DU; all other areas

compose the “outside” DU.



QuickTimeª and a TIFF (Uncompressed) decompressor

are needed to see this picture.

Figure 3: Sampling locations for YE rockfish. (A) Outside samples, (B)Inside samples. QB sampling locations (not shown) are comparable to

the YE sample locations.A.



B.





Figure 4: AFLP screening schematic. (1) Individual fish from the same

area will be pooled together. (2) Different groups will be screened foroutlier loci with many primer pairs. (3) Primer pairs that amplify outlierloci will be identified. (4) The groups will be screened at the individuallevel with the primer pairs known to amplify candidate loci.



ReferencesAgardy, M.T. (1994) Advances in marine conservation: the role of marine protectedareas. Trends in Ecology and Evolution (9)7 pp. 267-270.

Allison, G.W., Lubchencho, J., Carr, M.H. (1998) Marine reserves are necessary but not



sufficient for marine conservation. Ecological Applicatinos (8)1 Supplement pp. S79-S92.

Antao, T., Lopes, A., Lopes, R.J., Beja-Pereira, A., Luikart, G. (2008) LOSITAN: Aworkbench to detect molecular adaptation based on a Fst-outlier method. BMCBioinformatics (9)323, doi:10.1186/1471-2105-9-323

Beaumont, M.A. and Nichols, R.A. (1996) Evaluating loci for use in the geneticanalysis of population structure. Proceedings of the Royal Society of London, Series B(263) pp. 1619-1626.

Beaumont, M.A. and Balding, D.J. (2004) Identifying adaptive genetic divergenceamong populations from genome scans. Molecular Ecology (13) pp. 969-980.

Bonin, A., Taberlet, P., Miaud, C., Pompanon, F. (2006) Explorative genome scan todetect candidate loci for adaptation along a gradient of altitude in the common frog(Rana temporaria). Molecular Biology and Evolution (23)4 pp. 773-783.

Botsford, L.W., Castilla, J.C., Peterson, C.H. (1997) The management of fisheries andmarine ecosystems. Science (277) pp. 509-515. Carvalho, G.R., Hauser, L. (1994) Molecular genetics and the stock concept infisheries. Reviews in Fish Biology and Fisheries (4)3 pp. 326-350.

Castilla, J.C. and Bustamante, R.H. (1989) Human exclusion from rocky intertidal of Las Cruces, central Chile: effects on Durvillaea Antarctica (Phaeophyta, Durvilleales).Marine Ecology Progress Series (50) pp. 203-214.

Conover, D.O., Clarke, L.M., Munch, S.B., Wagner, G.N. (2006) Spatial and temporalscales of adaptive divergence in marine fishes and the implications for conservation.

Journal of Fish Biology (69) Supplement C, pp. 21-47.

COSEWIC 2002. COSEWIC assessment and status report on the Bocaccio Sebastes paucispinis in Canada. Committee on the Status of Endangered Wildlife in Canada.Ottawa.

COSEWIC. 2007. COSEWIC assessment and status report on the canary rockfishSebastes pinniger in Canada. Committee on the Status of Endangered Wildlife inCanada. Ottawa. (www.sararegistry.gc.ca/status/status_e.cfm).

COSEWIC. 2008. COSEWIC assessment and status report on the YE Rockfish Sebastesruberrimus, Pacific Ocean inside waters population and Pacific Ocean outside waterspopulation, in Canada. Committee on the Status of Endangered Wildlife in Canada.Ottawa. (www.sararegistry.gc.ca/status/status_e.cfm).

DeMartini, E.E. (1993) Modeling the potential of fishery reserves for managing Pacific

coral reef fishes. Fishery Bulletin (91) pp. 414-427.

Federal Register (2008) Listing Endangered and Threatened Species and DesignatingCritical Habitat: Notice on Finding on a Petition to List Five Rockfish Species in PugetSound (WA) as Endangered or Threatened Species Under the Endangered SpeciesAct.”73(52).

Halpern, B.S. and Warner, R.R. (2002) Marine reserves have rapid and lasting effects.



Ecology Letters (5) pp. 361-366.

Halpern, B.S. (2003) The impact of marine reserves: do reserves work and doesreserve size matter? Ecological Applications (13)1 Supplement, pp. S117-S137.Hamilton, S.L., Regetz, J., Warner, R.R. (2008) Postsettlement survival linked to larvallife in a marine fish. Proceedings of the National Academy of Sciences. (105)5 pp.

1561-1566.

Hauser, L. and Carvalho, G.R. (2008) Paradigm shifts in marine fisheries genetics:ugly hypotheses slain by beautiful facts. Fish and Fisheries (9) pp. 333-362.

Hemmer-Hansen, J., Nielsen, E.E., Frydenberg, J., Loeschcke, V. (2007) Adaptivedivergence in a high gene flow environment: Hsc70 variation in the Europeanflounder (Platichthys flesus L.) Heredity (99) pp. 592-600.

Hughes, T.P., Bellwood, D.R., Foke, C., Steneck, R.S., Wilson, J. (2005) New paradigmsfor supporting the resilience of marine ecosystems. Trends in Ecology and Evolution(20)7 pp. 380-386.

Hyde J.R. and Vetter, R.D. (2007) The origin, evolution, and diversification of rockfishes of the genus Sevastes (Cuvier). Molecular Phylogenetics and Evolution (44)pp. 790-811.

Gagnaire, P.A., Albert, V., Jonsson, B., Bernatchez, L. (2009) Natural selectioninfluences AFLP intraspecific variability and introgression patterns in Atlantic eels.Molecular Ecology (18) pp. 1678-1691.

Lea, R.N., McAllister, R.D. VenTresca, D. (1999) Biological aspects of nearshorerockfishes of the genus Sebastes from Central California. State of CaliforniaDepartment of Fish and Game Fish Bulletin (177).

Levin, L.A. (2006) Recent progress in understanding larval dispersal: new directionsand digressions. Integrative and Comparative Biology 46(3) pp. 282-297.

Lotze, H.K., Lenihan, H.S., Bourque, B.J., Bradbury, R.H., Cooke, R.G., Kay, M.C.,Kidwell, S.M., Kirby, M.X., Peterson, C.H., Jackson, J.B.C. (2006) Depletion,degradation and the recovery potential of estuaries and coastal seas. Science(312)5781 pp. 1806-1809.

Love, M.S., Yoklavich, M., Thorsteinson, L. (2002) The Rockfishes of the NortheastPacific. University of California Press, Los Angeles.

Lubchenco, J., Palumbi, S.R., Gaines, S.D., Andelman, S. (2003) Plugging a hole in theocean: the emerging science of marine reserves. Ecological Applications (13)1Supplement, pp. S3-S7.

McKay, J.K. and Latta, R.G. (2002) Adaptive population divergence: markers, QTL andtraits. Trends in Ecology and Evolution (17), pp. 285-291.

Palumbi, S.R. (1994) Genetic divergence, reproductive isolation, and marinespeciation. Annual Review of Ecology and Systematics (25) pp. 547-572.

Palumbi, S.R. (2003) Population genetics, demographic connectivity, and the designof marine reserves. Ecological Applications (13)1 Supplement, pp. S146-S158.



Parker, S.J., Berkeley, S.A., Golden, J.T., Gunderson, D.R., Heifetz, J., Hixon, M.A.,Larson, R., Leaman, B.M., Love, M.S., Musick, J.A., O’Connell, V.M., Ralston, S., Weeks,H.J., Yoklavich, M.M. (2000) Management of Pacific Rockfish. Fisheries (25)3 pp. 22-29.

Rabalais, N.N., Turner, R.E., Diaz, R.J., Justic, D. (2009) Global change and

eutrophication of coastal waters. ICES Journal of Marine Science (66) pp. 1528-1537.

Selkoe, K.A., Henzler, C.M., Gaines, S.D. (2008) Seascape genetics and the spatialecology of marine populations. Fish and Fisheries (9) pp. 363-377.

Slatkin, M. (1973) Gene flow and selection in a two-locus system. Genetics (81) pp.787-802.

Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A.,Pot, J., Peleman, J., Kuiper, M. et al. (1995) AFLP: a new technique for DNAfingerprinting. Nucleic Acids Research (23)21 pp. 4407-4414.

Waples, R.S. (1998) Separating the wheat from the chaff: patterns of geneticdifferentiation in high gene flow species. Genetics (89), pp. 438-450.

Ward, R.D., Woodwark, M., Skibinski, D.O.F. (1994) A comparison of genetic diversitylevels in marine, freshwater and anadromous fishes. Journal of Fish Biology (44)2 pp.213-232.

Warner, R.R. and Cowen, R.K. (2002) Local retention of production in marinepopulations: evidence, mechanisms, and consequences. Bulletin of Marine Science70(1) Supplement, pp. 245-259.

Whitlock, M.C. and McCauley, D.E. (1999) Indirect Measures of gene flow andmigration: Fst ≠ 1/(4Nm+1) Heredity (82) pp. 117-125.

Worm, B., Barbier, E.B., Beaumont, N., Duffy, J.E., Folke, C., Halpern, B.S., Jackson, J.B.C., Lotze, H.K., Micheli, F., Palumbi, S.R., Sala, E., Selkoe, K.A., Stachowicz, J.J.,Watson, R. (2006) Impacts of biodiversity loss on ocean ecosystem services. Science(314) pp. 787-790.

Wright, S. (1931) Evolution in Mendelian populations. Genetics (16) pp. 97-159.

Yamanaka, K.L. and Lacko, L.C. 2001. Inshore Rockfish (Sebastes ruberrimus, S.maliger, S. caurinus, S. melanops, S. nigrocinctus, and S. nebulosus) StockAssessment for the West Coast of Canada and Recommendations for Management.Canadian Science Advisory Secretariat Research Document 2001/139.

Yamanaka, K.L., Lacko, L.C., Withler, R., Grandin, C., Lockhead, J.K., Martin, J.C.,Olsen, N., Wallace, S.S. (2006a) A review of YE rockfish Sebastes ruberrimus along

the Pacific coast of Canada: biology, distribution and abundance trends. CanadianScience Advisory Secretariat . Research Document 2006/076.

Yamanaka, K.L., Lacko, L.C., Miller-Saunders, K., Grandin, C., Lochead, J.K., Martin, J.C., Olsen, N., Wallace, S.S. (2006b) A review of QB rockfish, Sebastes maliger , alongthe Pacific coast of Canada: biology, distribution and abundance trends. CanadianScience Advisory Secretariat . Research Document 2006/nnn.

Zhivotovsky, L. (1999) Estimating population structure in diploids with multilocus



dominant markers. Molecular Ecology (8) pp. 907-913.

Signals of Adaptive Genetic Variation in BC’s Nearshore Rockfish: Implications

Documents

Transcript of Signals of Adaptive Genetic Variation in BC’s Nearshore Rockfish: Implications