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Selection and sex-biased dispersal in a coastal shark: The influence of philopatry on adaptive variation


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Sex-biased dispersal is expected to homogenize nuclear genetic variation relative to variation in genetic material inherited through the philopatric sex. When site fidelity occurs across a heterogeneous environment, local selective regimes may alter this pattern. We assessed spatial patterns of variation in nuclear-encoded, single nucleotide polymorphisms (SNPs) and sequences of the mitochondrial control region in bonnethead sharks (Sphyrna tiburo), a species thought to exhibit female philopatry, collected from summer habitats used for gestation. Geographic patterns of mtDNA haplotypes and putatively neutral SNPs confirmed female philopatry and male-mediated gene flow along the northeastern coast of the Gulf of Mexico. A total of 30 outlier SNP loci were identified; alleles at over half of these loci exhibited signatures of latitude-associated selection. Our results indicate that in species with sex-biased dispersal, philopatry can facilitate sorting of locally adaptive variation, with the dispersing sex facilitating movement of potentially adaptive variation among locations and environments. This article is protected by copyright. All rights reserved.
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Selection and sex-biased dispersal in a coastal shark: the
influence of philopatry on adaptive variation
*Department of Life Sciences, Marine Genomics Laboratory, Harte Research Institute, Texas A&M University-Corpus Christi,
6300 Ocean Drive, Corpus Christi, TX 78412, USA, University of North Florida, 1 UNF Drive, Jacksonville, FL 32224, USA,
Stony Brook University, Stony Brook, NY 11776, USA
Sex-biased dispersal is expected to homogenize nuclear genetic variation relative to
variation in genetic material inherited through the philopatric sex. When site fidelity
occurs across a heterogeneous environment, local selective regimes may alter this pattern.
We assessed spatial patterns of variation in nuclear-encoded, single nucleotide polymor-
phisms (SNPs) and sequences of the mitochondrial control region in bonnethead sharks
(Sphyrna tiburo), a species thought to exhibit female philopatry, collected from summer
habitats used for gestation. Geographic patterns of mtDNA haplotypes and putatively
neutral SNPs confirmed female philopatry and male-mediated gene flow along the north-
eastern coast of the Gulf of Mexico. A total of 30 outlier SNP loci were identified; alleles
at over half of these loci exhibited signatures of latitude-associated selection. Our results
indicate that in species with sex-biased dispersal, philopatry can facilitate sorting of
locally adaptive variation, with the dispersing sex facilitating movement of potentially
adaptive variation among locations and environments.
Keywords: elasmobranchs, genome scan, localized adaptation, male-mediated gene flow
Received 13 July 2015; revision received 27 October 2015; accepted 27 October 2015
Sex-biased dispersal arises when individuals of one sex
exhibit site fidelity (philopatry), while individuals of
the opposite sex are prone to disperse (Pusey 1987).
This occurs in a wide variety of vertebrate taxa (e.g.
birds, Clarke et al. 1997; mammals, Lawson Handley &
Perrin 2007) and is thought to result from fitness differ-
ences between the sexes associated with local competi-
tion for resources (including mates), inbreeding
avoidance, and/or parental investment (Gandon 1999;
Perrin & Mazalov 2000). There also is a relationship
between mating system and which sex is dispersive;
monogamous species feature territorial males and dis-
persive females, while polygamous species feature
female philopatry and male dispersal (Greenwood
Dispersal and resulting gene flow acts as a homoge-
nizing force across the genome, opposed by the pro-
cesses of genetic drift and disruptive selection. The
level of gene flow necessary to counteract genetic drift
can be relatively small, as large populations experience
little drift and only a few migrants are required in small
populations (Wright 1931; Slatkin 1985). Disruptive
selection, on the other hand, is capable of generating
divergence in specific genomic regions, even when gene
flow is high, if the strength of selection is high relative
to the number of immigrants and/or the patterns of
immigration are nonrandom in relation to local environ-
mental conditions (Endler 1973; Slatkin 1987; Garant
et al. 2007). Sex-biased dispersal, via gene flow through
the dispersive sex, has a homogenizing effect on bipar-
entally inherited nuclear variation; uniparentally
inherited markers not under disruptive selection (e.g.
heterologous sex chromosomes, mtDNA) sort through
the philopatric sex and may depart from homogeneity
at a greater rate through time (Avise 1994). If habitats of
a philopatric species vary in environmental conditions,
Correspondence: David S. Portnoy, Fax: 361-825-2025; E-mail:
©2015 John Wiley & Sons Ltd
Molecular Ecology (2015) 24, 5877–5885 doi: 10.1111/mec.13441
the homogenizing effects of sex-mediated gene flow
may be counteracted in specific genomic regions if
localized selection leads to increased reproductive suc-
cess for the philopatric sex (Lenormand 2002). Finally,
philopatric behaviour by one of the sexes can reduce
the strength of migration, facilitating local adaptation
(Slatkin 1987).
Studies in several species of live-bearing sharks have
revealed spatial genetic patterns (homogeneity in
nuclear-encoded microsatellites and heterogeneity in
maternally inherited mtDNA) consistent with female
philopatry and male-mediated gene flow (Portnoy &
Heist 2012; Chapman et al. 2015). Females in these spe-
cies exhibit considerable parental investment, giving
birth after long gestation periods to small litters of fully
developed offspring, suggesting that return to a favour-
able habitat could enhance embryonic growth during
gestation (Economakis & Lobel 1998; Driggers et al.
2014) as well as provide predictable access to food and
shelter from predators (Heupel et al. 2007). It also is
known that habitats used by the same species for gesta-
tion and/or parturition may differ substantially, even at
small spatial scales (DiBattista et al. 2007; Feldheim et al.
2014). Based on the above, coastal philopatric sharks
represent a good model system to assess possible effects
that localized adaptation may have on genomewide pat-
terns of variation in the context of sex-asymmetric gene
We assessed spatial patterns of variation in nuclear-
encoded single nucleotide polymorphisms (SNPs) and
sequences of the mitochondrial control region in bon-
nethead sharks (Sphyrna tiburo), a species thought to
exhibit female-biased philopatry (Driggers et al. 2014).
Bonnetheads are common seasonal residents in coastal
and estuarine waters of the western Atlantic Ocean
(Atlantic), including the Gulf of Mexico (Gulf), and are
known to use nearshore habitat for gestation and partu-
rition (Compagno 1984; Driggers et al. 2014). Bonnet-
heads in the Atlantic and Gulf migrate seasonally, and
a variety of life stages are commonly found in bays,
estuaries, and nearshore waters from May to November
(Cortes et al. 1996; Ulrich et al. 2007). The species has a
short gestation period of 45 months (Parsons 1993),
with parturition occurring in the late summer to early
fall and mating occurring shortly thereafter (Manire &
Rasmussen 1997; Ulrich et al. 2007). Sperm storage is
necessary, as ovulation does not occur until spring
(Manire et al. 1995). Bonnetheads mature between
17 years (Lombardi-Carlson et al. 2003; Frazier et al.
2014) and females give birth to 214 (avg. ~9) fully
developed pups (Frazier et al. 2013). Unlike other
coastal sharks, the observed migratory behaviour does
not appear to be associated with the use of nursery
areas (Heupel et al. 2007), but instead may be related to
increasing food availability for gestating females and
gaining access to potential mates for males (Driggers
et al. 2014). Significant differences in life history among
bonnetheads across small geographic regions have been
documented in several studies; differences found
between samples from the eastern Gulf include size at
age, growth rate, and size and age at maturity (Parsons
1993; Carlson & Parsons 1997; Lombardi-Carlson et al.
2003). In addition, studies in both the Atlantic and east-
ern Gulf have shown site fidelity by adult bonnetheads
(particularly females) to particular estuaries or bays
during the summer months, on intra- and interannual
timescales (Heupel et al. 2006; Driggers et al. 2014).
We sampled adult and subadult animals from three
localities along the west coast of Florida (eastern Gulf
of Mexico) and one locality off the coast of North Caro-
lina (western Atlantic Ocean). Sample localities in the
Gulf were selected because of identified latitudinal dif-
ferences in life history parameters among bonnetheads
in the region (Lombardi-Carlson et al. 2003); the sample
from the Atlantic was included to have a sample out-
side the Gulf and because of identified differences in
life history between bonnetheads in the Gulf and Atlan-
tic (Frazier et al. 2014). We used a ddRAD approach
(Peterson et al. 2012) to genotype individuals at thou-
sands of nuclear-encoded SNPs, permitting a search for
spatial differences in genomic regions putatively under
selection; inclusion of putatively neutral SNPs and
mtDNA sequences allowed us to assess further whether
dispersal in bonnetheads is sex-biased.
Materials and methods
Tissues (fin clips) from 134 bonnetheads sampled
between 1998 and 2000 from four nearshore localities
(Fig. 1) were used in the study. Samples were obtained
during the summer months (May to September) when
mature individuals are in areas used for gestation, par-
turition, and mating. Individuals sampled were mostly
a mix of mature females and males.
Double-digest RAD (ddRAD) libraries were prepared
following Peterson et al. (2012); details of the protocol
may be found in the Appendix S1 (Supporting informa-
tion). Libraries were sequenced on two lanes of an Illu-
mina HiSeq 2000 DNA sequencer. The first library was
sequenced as a paired-end run for reference contig
assembly in order to facilitate downstream bioinformat-
ics inference. The second library was sequenced as a
single-end run, as a cost-effective manner to genotype
SNPs. The dDocent pipeline (Puritz et al. 2014) was used
for reference contig assembly, read mapping, and SNP
genotyping. Default parameters were used for each
step, with the exception of contig assembly, where a
customized script was used to mitigate the high levels
©2015 John Wiley & Sons Ltd
of repeats and duplications expected in large genomes.
The initial set of data consisted of 648 035 variant SNP
loci across 147 920 fragments.
The entire mitochondrial control region (1134 bp) was
amplified using primers Pro-L and 282H (Keeney et al.
2003); details of the protocol may be found in the
Appendix S1 (Supporting information). Electrophore-
tograms were examined by eye, aided by GENEIOUS v.7.1
(Biomatters Ltd.); all sequences were trimmed to
1064 bp due to occasional nonspecific amplification on
the 30end that made accurate base calling difficult.
Single nucleotide polymorphisms were extensively fil-
tered before further analysis. The initial raw data set
was filtered to remove all genotypes with <5 reads per
individual and loci called in <75% of all individuals.
Consequently, only the top 90% of individuals in geno-
type call rate were retained. The resulting data set con-
tained 121 individuals. SNPs were then filtered to meet
the following criteria: presence in 97.5% of individuals
across the data set, minor allele frequency >5% across
the data set, and conformance to expectations of
HardyWeinberg equilibrium (HWE). Additional
parameters considered during filtering included allele
balance within heterozygous individuals, SNP quality
to depth ratio, percentage of contribution from forward
and reverse reads, maximum mean read depth across
individuals, and removal of possible paralogs (Details
on SNP filtering are described in Appendix S1, Sup-
porting information). The final, filtered data set con-
sisted of 5914 SNPs spread across 3967 fragments.
Genetic diversity (nuclear genome) within each locality
was assessed as the mean nucleotide diversity (p) across
all SNPs, using VCFTOOLS (Danecek et al. 2011). Homo-
geneity of pacross localities was assessed using analysis
of variance (ANOVA) and TukeyKramer HSD indepen-
dent contrasts as implemented in JMP
v.11 (SAS Institute
Inc.). Genetic diversity (mtDNA) was assessed as mean
nucleon (h) and nucleotide diversity (p) within each
80° W86° W
27° N 32° N
Fig. 1 Samples of bonnethead sharks obtained off North Carolina (NC, blue), Florida Bay (FB, red; 18 males, 13 females), Tampa Bay
(TB, orange; 17 males, 14 females) and Panama City (PC, yellow; 15 males, 21 females). Results of discriminant analysis of principle
components for (A) putatively neutral N-SNP loci, (B) outlier O-SNP loci putatively under selection, with group membership defined
by sample locality, and (C) outlier O-SNP loci putatively under selection, with group membership based on k-means clustering.
Females are coded as circles, males as triangles, and individuals of unknown sex as squares. Representative allele frequencies (D) of
three O-SNP loci (left to right, E66074, E109425, E106435) that contributed ~24% to the distribution of individuals along the X-axis.
Colours represent sample locations for all figures. SNP, single nucleotide polymorphism.
©2015 John Wiley & Sons Ltd
locality, using ARLEQUIN v. (Excoffier & Lischer
Relatedness of individuals within each locality was
assessed in VCFTOOLS, using the statistic developed by
Yang et al. (2010). Two individuals in the sample from
Florida Bay (FB) possessed high relatedness to each other
(0.61) relative to the average relatedness (0.045) across
all individuals, suggesting these two individuals shared
parents. The individual with more missing data was
removed from subsequent SNP-based analyses to avoid
possible issues with consanguinity. SNPs were then orga-
nized into haplotypes (loci), using a custom Perl script
that produces output in GENEPOP format. During haplo-
typing, a total of 23 loci were excluded from further anal-
ysis; 12 were identified as possible paralogs and 11 could
not be haplotyped in more than 90% of individuals
assayed. GENEPOP files were converted to BAYESCAN format,
using PGDSPIDER v.2.0.7 (Lischer & Excoffier 2012), and
BAYESCAN (Foll & Gaggiotti 2008) was used to identify
individual outlier loci by assessing fit to different models
of selection. The program was run with all default values,
with the exception of 30 pilot runs and a thinning interval
of 50; significance of outlier loci was determined using a
q-value that directly corresponded to a false discovery
rate (FDR) of 0.05. Loci were then divided into two sets:
one that contained putatively neutral SNPs (N-SNP loci)
and one that contained outlier SNPs (O-SNP loci) puta-
tively under selection.
Geographic homogeneity among localities in N-SNP
and O-SNP loci was tested using single-level analysis of
molecular variance (AMOVA), as implemented in GENODIVE
V.2.0 (Meirmans & van Tienderen 2004). Pairwise F
values (both nuclear data sets) were estimated using
GENODIVE; significance of pairwise F
values was
assessed by permuting individuals between samples
10 000 times. Homogeneity of mtDNA haplotypes
among localities was tested using single-level AMOVA,as
implemented in ARLEQUIN. Distances were calculated
using a Kimura 2-parameter model (Kimura 1980), as
selected by JMODELTEST v. 2.1.4 (Guindon & Gascuel
2003; Darriba et al. 2012). Pairwise Φ
values were esti-
mated using ARLEQUIN, with significance determined by
permuting individuals between samples 10 000 times.
Correction for multiple testing was implemented using
the FDR procedure (Benjamini & Hochberg 1995).
Discriminant Analysis of Principle Components
(DAPC; Jombart et al. 2010) was carried out on both
N-SNP and O-SNP loci, using the ADEGENET package
(Jombart & Ahmed 2011) in Rv.3.0.2 (R Development
Core Team 2013), with group membership defined by
locality. DAPC also was carried out on O-SNP loci,
with group membership inferred using k-means cluster-
ing (MacQueen 1967); contribution of O-SNP loci to
genetic clustering was then inferred from loading vari-
ables used in each discriminant function. For all O-SNP
loci, the reference contig, assembled from paired-end
reads, was screened against the NCBI nucleotide-read
database, using the BLASTN algorithm (Altschul et al.
1990). The top three hits with E-values <0.01 were
Summary statistics for SNPs and mtDNA are given in
Table S1 (Supporting information); GenBank accession
numbers and geographic distribution of mtDNA haplo-
types are given in Table S2 (Supporting information).
Estimated mean nucleotide diversity (p) across all SNP
loci per sample (SE) varied from 0.296 (0.002) in the
sample from North Carolina (NC) to 0.319 (0.002) in
the sample from FB. Mean estimates of pdiffered sig-
nificantly across samples (F
=21.483, P<0.001), with
mean pin NC being significantly lower than in the
other samples (TukeyKramer HSDP<0.001). The
same pattern was observed in haplotype diversity of
mtDNA sequences; estimated diversity was lower in
NC (h=0.719 0.077), while hvalues did not differ
among the other three samples.
A total of 30 haplotypes, containing 49 O-SNPs, were
identified as candidate loci under selection (q<0.05);
the remaining SNPs (5865 scattered across 3910 haplo-
types) were consistent with a neutral model. A total of
72 alleles were identified among the 30 O-SNP loci; 21
loci were bi-allelic, while nine were multi-allelic
(Table S3, Supporting information). Significant hetero-
geneity among all four localities in all three marker
types was detected by AMOVA (Table S4, Supporting
information); the proportion of the total genetic vari-
ance explained by geography (locality) was 0.79%
(N-SNP loci), 7.77% (mtDNA haplotypes), and 27.07%
(O-SNP loci). Pairwise estimates of F
and Ф
(Table 1) revealed differences among the three marker
types. For N-SNP loci, allele frequencies in NC differed
significantly from those in FB, TB (Tampa Bay), and PC
(Panama City); allele frequencies in the latter three were
homogeneous. For mtDNA, the haplotype distribution
in NC differed significantly from those in FB, TB, and
PC; estimates of Ф
between FB and PC differed signif-
icantly from one another, while those between FB and
TB and TB and PC were homogeneous. Allele frequen-
cies of O-SNP loci in both NC and PC differed signifi-
cantly from one another and from those in FB and TB,
while allele frequencies in FB and TB were homoge-
neous. Significant heterogeneity among the three locali-
ties in the Gulf also was detected by AMOVA for mtDNA
haplotypes (F
=0.027, P=0.033) and O-SNP loci
=0.157, P=0.000), but not for N-SNP loci
=0.0003, P=0.151).
©2015 John Wiley & Sons Ltd
Analysis of N-SNP loci, using DAPC and with prior
group membership defined by locality, revealed two
distinct clusters along the primary (X) axis (Fig. 1A);
one was comprised of individuals from NC, while the
other contained individuals from the three localities in
the Gulf. Analysis of O-SNP loci, with prior group
membership defined by locality, revealed a different
pattern along the primary axis (Fig. 1B). Twelve
individuals from PC clustered with individuals in the
sample from NC, while the remaining individuals
formed a second cluster; both clusters were more
diffuse than in the analysis of N-SNP loci. When prior
group membership of O-SNP loci was inferred using k-
means clustering, three distinct clusters were revealed
in DAPC analysis (Fig. 1C). One cluster contained pri-
marily individuals from NC and PC and one individual
from TB; one cluster contained individuals from the
Gulf, primarily from PC; and one cluster contained
mostly individuals from FB and TB and one individual
from PC. The primary (X) axis described 99.6% of the
variance. Allele frequencies at three representative O-
SNP loci (Fig. 1D) clearly reveal a clinal, northsouth
(latitudinal) pattern in allele frequencies. The correla-
tion between allele (haplotype) frequencies at each O-
SNP locus and latitude was then evaluated using stan-
dard least squares regression as implemented in JMP
v.11. Alleles at 17 O-SNP loci were correlated (P0.05)
with latitude and explained 56.9% of the variation
along the primary axis, while 18 O-SNP loci had r
ues 0.90 and explained 75.6% of the variation along
the X.
Eight of the 30 O-SNP loci had no sequence counter-
part in GenBank; the remaining 22 were highly similar
(E-value <0.01) to several DNA sequences (Table S5,
Supporting information). Frequent ‘hits’ included
sequence similarities to clones or contigs in other spe-
cies, and to annotated genomic regions of known
immune response proteins (e.g. cytokines MIP-3 and
interleukin-1band a T cell receptor), putative regulatory
elements (e.g. zinc-finger proteins, Hox genes), and
SINE-type sequences.
The significant difference in N-SNP loci between bon-
netheads from the Atlantic and Gulf indicates geneti-
cally distinct populations with little to no gene flow
between the two regions. This geographic pattern has
been observed in other marine taxa (Avise 1992; Gold &
Richardson 1998; Gold et al. 2009) including coastal
sharks (Portnoy et al. 2014) and supports results from a
recent mtDNA assessment of population structure in
the bonnethead (Escatel-Luna et al. 2015). This pattern
is hypothesized to stem from biogeographic processes
associated with the Florida Current and/or narrowing
of the continental shelf in southeastern Florida (Portnoy
et al. 2014). The absence of significant divergence in
N-SNP loci among the three localities in the Gulf is con-
sistent with gene flow occurring between the Florida
Keys (FB) and north-central Florida (PC).
Asymmetry in geographic patterns of variation
between N-SNP loci (homogeneous) and mtDNA haplo-
types (heterogeneous) among bonnetheads from the
Gulf is consistent with female philopatry and male-
biased dispersal (Melnick & Hoelzer 1992). Because
mtDNA is haploid and uniparentally inherited, a
greater magnitude of divergence at mtDNA compared
to nuclear loci is to be expected (Birky 2001). Similar
patterns are documented in several shark species (Port-
noy & Heist 2012; Chapman et al. 2015) and interannual
tag-and-recapture studies of bonnetheads (Driggers
et al. 2014) demonstrate strong site fidelity of females to
specific estuaries. The pattern of mtDNA haplotype
variation among bonnetheads in the Gulf indicates an
isolation-by-distance effect rather than complete isola-
tion as mtDNA haplotypes in the intermediate sample
locality (TB) did not differ significantly from those in
sample localities (PC and FB) at the geographic
extremes. This also suggests that female bonnetheads
may stray from preferred localities but most likely to
neighbouring ones.
The largest proportion of the genetic variance explained
by locality (geography) was due to O-SNP loci. In theory,
Table 1 Below diagonal: pairwise F
values for putatively neutral SNP loci (N-SNP) and for outlier SNP loci putatively under
selection (O-SNP), and pairwise Φ
values for mtDNA haplotypes (mtDNA), between samples of bonnetheads obtained off North
Carolina (NC), Florida Bay (FB), Tampa Bay (TB) and Panama City (PC). Above diagonal: probability (P) values; those significant
after correction for multiple comparisons are given in bold
NC <0.001 <0.001 <0.001 NC <0.001 <0.001 <0.001 NC <0.001 0.001 0.014
FB 0.019 0.317 0.038 FB 0.543 0.382 <0.001 FB 0.234 0.158 0.011
TB 0.021 0.000 0.344 TB 0.462 0.000 <0.001 TB 0.161 0.014 0.406
PC 0.021 0.001 0.000 PC 0.180 0.244 0.177 PC 0.064 0.055 0.000
©2015 John Wiley & Sons Ltd
outlier loci can reflect genomic regions associated with
local adaptive differences (Nielsen et al. 2009; Allendorf
et al. 2010) or genomic regions that have diverged more
than expected over time via a nonadaptive process such
as genetic drift (Hedrick 2011). However, genetic drift is a
genomewide effect (Luikart et al. 2003) and the significant
correlations between allele frequencies at O-SNP loci and
latitude and the complete absence of any clinal pattern in
N-SNP loci indicate that the observed geographic pattern
of O-SNP loci stems from localized divergent selection.
The greater similarity in allele frequencies at outlier
O-SNP loci between PC and NC also supports divergent
selection associated with latitude as the two localities are
situated at more northerly latitudes yet are at the geo-
graphic extreme of possible (homogenizing) gene flow
among the localities studied.
Signatures of latitude-driven selection are common
given that natural phenomena (e.g. climate, diurnal
cycle) impact distributions of biological organisms, and
that selection is imposed by the local biotic environment
and interactions between a focal population and other
organisms (Kawecki & Ebert 2004). Examples of well-
known latitude-specific effects on marine fish include
demographic traits such as growth rate (Conover & Pre-
sent 1990) and hostparasite/pathogen systems (Poulin
& Morand 2000). A few of the O-SNP loci found in this
study did have sequence similarities to regions of genes
putatively involved in regulation and development, and
there are significant latitudinal differences in growth rate
and size at age among bonnetheads in the region of the
Gulf sampled (Lombardi-Carlson et al. 2003). A larger
proportion of the O-SNP loci had sequence similarities to
regions of genes involved in immune response. This
result might reflect latitudinal variation in parasite infec-
tivity (Poulin & Morand 2000) and increased infectivity
of parasites to sympatric hosts rather than allopatric
hosts of the same species (Morand et al. 1996). Some cau-
tion in interpreting these data, however, is advisable, in
part because the O-SNP loci sequences were small in size,
and in part because the majority of SNPs recovered using
a ddRAD approach are not within protein-coding genes
(Baxter et al. 2011). Further, while we found a general
correlation of allele frequencies with latitude for O-SNPs,
this does not demonstrate causation as other factors may
be equally or more important. As an example, the spatial
sampling encompasses both the warm-temperate and
tropical provinces along the Florida coast, and differ-
ences in allele frequencies could reflect differences in
ecology and climate.
Occurrence of philopatry in association with a non-
random pattern of geographic variation in small geno-
mic regions was reported recently (Stiebens et al. 2013)
in a study of variation in MHC alleles among philopa-
tric loggerhead turtles in the Cape Verde Archipelago.
Both mtDNA haplotypes and MHC alleles were struc-
tured genetically among nesting islands, but only
nuclear-encoded microsatellites followed a geographic
pattern, in this case one of isolation by distance indica-
tive of restricted male dispersal. In our study, only
females appeared structured geographically along the
western coast of Florida. These and tagging data
(Driggers et al. 2014) where >95% of interannual bonnet-
head returns to the same estuary were female indicate
that bonnethead males are less philopatric than females,
and that maintenance of localized adaptive alleles in
bonnetheads may occur through female matrilines.
Thus, selection and sex-specific philopatry can interact
to sort adaptive nuclear alleles across geographic space.
Association of spatially discrete matrilines and local-
ized genomic regions under selection suggest that
female genotype and philopatry to gestational areas
may increase offspring fitness as a maternal effect
(Mousseau & Fox 1998; Badyaev & Uller 2009). This is
consistent with a review of parental effects in species
with sex-asymmetric dispersal and a model that
showed that selective pressure to develop locally adap-
tive parental effects is high when dispersal is sex-biased
(Revardel et al. 2010). Unfortunately, studies of parental
effects in sharks are limited (Hussey et al. 2010) despite
a female reproductive biology (long gestation, live
birth) in several species that suggests occurrence of
important maternal effects.
Sex-specific philopatry reduces overall dispersal and
consequently may redistribute genetic diversity among
rather than within subpopulations or demes. In bonnet-
head sharks, homogeneity of N-SNP loci across geo-
graphic localities within the Gulf demonstrates that
genetic diversity was partitioned equally within and
among demes, indicating that extensive male dispersal
was enough to overcome drift processes. In contrast,
strong differentiation at a small subset of nuclear genes
among samples collected at gestational areas indicates
that localized selection was sufficiently strong to out-
weigh the homogenizing force of dispersal and gene
flow. Thus, while female philopatry in bonnethead
sharks may promote maintenance of adaptive alleles in
specific localities, gene flow mediated by males or stray-
ing females could move potentially adaptive variation
among environments (Slatkin 1987; Garant et al. 2007).
Given local environmental heterogeneity on larger tem-
poral scales, the maintenance and movement of poten-
tially adaptive variation across the landscape likely
facilitates species persistence (Bowen & Roman 2005).
We thank C.A. Manire for providing several samples from
Florida and P. Bentzen and two anonymous reviewers for
©2015 John Wiley & Sons Ltd
helpful comments and suggestions. This work was supported
by funds provided by the College of Science and Engineering
at Texas A&M University-Corpus Christi and by the Environ-
mental Protection Agency (Award #R826128-01-0 to C.A. Man-
ire). Although the research described in this article was
supported in part by the United States Environmental Protec-
tion Agency, it has not been subjected to the agency’s required
peer and policy review and therefore does not necessarily
reflect the views of the Agency and no official endorsement
should be inferred. Field sampling in Florida was conducted
under research permits issued by the Florida Fish and Wildlife
Conservation Commission to Mote Marine Laboratory. This
article is publication number 10 of the Marine Genomics
Laboratory at Texas A&M University-Corpus Christi and
number 104 in the series Genetic Studies in Marine Fishes.
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D.S.P., J.B.P. and J.R.G. had responsibility for data col-
lection and analysis and primary responsibility for writ-
ing of the manuscript. All other authors have reviewed
and contributed to the current version of the manu-
script. C.M.H. participated in data collection and
analysis, and J.G. and D.C. obtained the samples.
Data accessibility
GenBank accession numbers for mtDNA sequences may
be found in Table S2 (Supporting information). Demulti-
plexed, raw sequencing reads: Short Read Archive (Bio-
project accession #PRJNA286089). The final SNP data set,
in VCF format, the neutral and outlier haplotype data
sets, in GENEPOP format, and a script to reproduce bioin-
formatic filtering: Dryad doi:10.5061/dryad.7k4c1.
Supporting information
Additional supporting information may be found in the online ver-
sion of this article.
Table S1 Summary of diversity statistics for 5914 SNPs and
sequences (1064 base pairs) of the mitochondrial control region
for samples of bonnetheads from North Carolina (NC) and
three localities along the Gulf Coast of Florida: Florida Bay
(FB), Tampa Bay (TB), and Panama City (PC).
Table S2 Distribution of haplotypes and GenBank Accession
numbers for mitochondrial control region sequences from sam-
ples of bonnetheads off North Carolina (NC) and three loca-
tions along the Gulf Coast of Florida: Florida Bay (FB), Tampa
Bay (TB) and Panama City (PC).
Table S3 Results of standard least squares regression of allele
frequencies at outlier loci by latitude: loci are organized as bi-
allelic and multi-allelic.
Table S4 Results of analysis of molecular variance (AMOVA) for
all three data sets.
Table S5 Results of BLAST search for sequence similarity of SNP
containing loci.
Appendix S1 Methods.
©2015 John Wiley & Sons Ltd
... It is also possible that philopatry might be sex biased as has been observed in Blacktip Sharks Carcharhinus limbatus (Keeney et al. 2005), lesser kestrels Falco naumanni (Alcaide et al. 2009), ringed salamanders Ambystoma annulatum (Williams et al. 2021), and several other animals. If one sex does not display philopatry, sufficient gene flow may be maintained between breeding habitats by the nonphilopatric sex, genetically homogenizing the population (Blundell et al. 2002;Portnoy et al. 2015). Channel Catfish may display male-biased philopatry because males build nests alone, mate monogamously, and provide uniparental care after driving off the female (Tatarenkov et al. 2006). ...
... Channel Catfish may display male-biased philopatry because males build nests alone, mate monogamously, and provide uniparental care after driving off the female (Tatarenkov et al. 2006). These conditions favor dispersal in females, potentially reducing breeding site fidelity and habitat segregation (Greenwood 1980;Portnoy et al. 2015). To test for sex-biased habitat preferences, we could estimate the genetic structure of Channel Catfish populations using sex-linked gene markers or observe differences between mitochondrial DNA (uniparental inheritance) and nuclear DNA (biparental inheritance) (Lawson Handley and Perrin 2007;Portnoy et al. 2015). ...
... These conditions favor dispersal in females, potentially reducing breeding site fidelity and habitat segregation (Greenwood 1980;Portnoy et al. 2015). To test for sex-biased habitat preferences, we could estimate the genetic structure of Channel Catfish populations using sex-linked gene markers or observe differences between mitochondrial DNA (uniparental inheritance) and nuclear DNA (biparental inheritance) (Lawson Handley and Perrin 2007;Portnoy et al. 2015). ...
Full-text available
Objective Individual habitat preference can reduce intraspecific competition for resources and may differ between age groups, sexes, and adult phenotypes. The Channel Catfish Ictalurus punctatus is a widespread species occurring in diverse freshwater habitats. This species displays breeding philopatry, returning to nesting sites occupied in previous years. Larger Channel Catfish tend to nest in the main channels of large rivers, whereas smaller fish tend to prefer smaller tributaries. The purpose of our study was to determine whether this habitat segregation potentially associated with habitat preference affects the genetic structure of a population. We hypothesized that spatial segregation of breeding sites in the Ottawa River and its smaller tributaries at Lac des Chats reduced gene flow within the population, resulting in genetically differentiated demes associated with lacustrine‐like and fluvial habitats. Methods Microsatellite allelic data was collected from 162 Channel Catfish. Result We found little genetic variation between the Ottawa, Mississippi, and Madawaska rivers. Furthermore, our analyses suggested that the sampled specimens comprised one panmictic population. Fish from one site in the Ottawa River, however, were significantly differentiated from fish from a nearby site also in the Ottawa River as well as from fish from the Mississippi River tributary. Conclusion Given that fish from sites further up the Ottawa River were not differentiated from fish from these sites, it is unlikely that geography can account for the differences observed; rather, assortative mating may explain the differentiation. We propose that panmixia within the population is caused by ontogenetic changes in habitat selection, straying individuals, or sex‐biased dispersal and philopatry.
... Therefore, natal philopatry could drive selection for locally adaptive phenotypes and lead to fine-scale adaptive structure (Portnoy et al., 2015;Portnoy & Heist, 2012). This could have further implications for management because parturition sites harbouring novel adaptive variants may require individually tailored policies. ...
... Gulf is consistent with previous assessments of mitochondrial DNA (Keeney et al., 2003 and life history traits such as maximum length and growth rate (Carlson et al., 2006). This observation is also consistent with studies of other marine fishes Leidig et al., 2015;Seyoum et al., 2017), including coastal sharks (Dimens et al., 2019;Portnoy et al., 2015Portnoy et al., , 2016, and aligns with the Florida Vicariance Zone (Neigel, 2009), where constriction of the continental shelf from Miami to West Palm Beach has reduced nearshore habitat (Avise, 1992;Neigel, 2009). Consequently, suitable parturition sites for coastal sharks are lacking in southeastern Florida and may dissuade female movement across the vicariance zone. ...
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Understanding how interactions among microevolutionary forces generate genetic population structure of exploited species is vital to the implementation of management policies that facilitate persistence. Philopatry displayed by many coastal shark species can impact gene flow and facilitate selection, and has direct implications for the spatial scales of management. Here, genetic structure of the blacktip shark (Carcharhinus limbatus) was examined using a mixed-marker approach employing mitochondrial control region sequences and 4339 SNP-containing loci generated using ddRAD-Seq. Genetic variation was assessed among young-of-the-year sampled in 11 sites in waters of the United States in the western North Atlantic Ocean, including the Gulf of Mexico. Spatial and environmental analyses detected 68 nuclear loci putatively under selection, enabling separate assessments of neutral and adaptive genetic structure. Both mitochondrial and neutral SNP data indicated three genetically distinct units-the Atlantic, eastern Gulf, and western Gulf-that align with regional stocks and suggest regional philopatry by males and females. Heterogeneity at loci putatively under selection, associated with temperature and salinity, was observed among sites within Gulf units, suggesting local adaptation. Furthermore, five pairs of siblings were identified in the same site across timescales corresponding with female reproductive cycles. This indicates that females re-used a site for parturition, which has the potential to facilitate the sorting of adaptive variation among neighbouring sites. The results demonstrate differential impacts of microevolutionary forces at varying spatial scales and highlight the importance of conserving essential habitats to maintain sources of adaptive variation that may buffer species against environmental change.
... Strong differentiation at these regions putatively under selection indicates that localized selection could be overpowering the homogenizing force of male dispersal. These patterns of malemediated dispersal and signatures of local selection are consistent with the hypothesis advanced by Portnoy et al. [44] that the combination of philopatric females and dispersing males may favor local adaptation by simultaneously allowing dispersal and the localized sorting of adaptive alleles. ...
... SNPs in nuclear RAD loci were extensively filtered before analysis using a workflow (see Additional file 3 for detailed SNP filtering workflow) based on the dDocent protocol [145] and following recommendations from O'Leary et al. [147] and Portnoy et al. [44]. In summary, the initial dataset of 49,028 SNPs output from FreeBayes was first filtered to remove all genotypes with < 5 reads per individual, quality scores < 25, and loci called in < 50% of individuals. ...
Full-text available
Background Reef manta rays ( Mobula alfredi ) are globally distributed in tropical and subtropical seas. Their life history traits (slow growth, late maturity, low reproductive output) make them vulnerable to perturbations and therefore require informed management strategies. Previous studies have reported wide-spread genetic connectivity along continental shelves suggesting high gene flow along continuous habitats spanning hundreds of kilometers. However, in the Hawaiian Islands, tagging and photo-identification evidence suggest island populations are isolated despite proximity, a hypothesis that has not yet been evaluated with genetic data. Results This island-resident hypothesis was tested by analyzing whole mitogenome haplotypes and 2048 nuclear single nucleotide polymorphisms (SNPs) between M. alfredi (n = 38) on Hawaiʻi Island and Maui Nui (the 4-island complex of Maui, Molokaʻi, Lānaʻi and Kahoʻolawe). Strong divergence in the mitogenome ( Φ ST = 0.488) relative to nuclear genome-wide SNPs (neutral F ST = 0.003; outlier F ST = 0.186), and clustering of mitochondrial haplotypes among islands provides robust evidence that female reef manta rays are strongly philopatric and do not migrate between these two island groups. Combined with restricted male-mediated migration, equivalent to a single male moving between islands every 2.2 generations (~ 64 years), we provide evidence these populations are significantly demographically isolated. Estimates of contemporary effective population size ( N e ) are 104 (95% CI: 99–110) in Hawaiʻi Island and 129 (95% CI: 122–136) in Maui Nui. Conclusions Concordant with evidence from photo identification and tagging studies, these genetic results indicate reef manta rays in Hawaiʻi have small, genetically-isolated resident island populations. We hypothesize that due to the Island Mass Effect, large islands provide sufficient resources to support resident populations, thereby making crossing deep channels separating island groups unnecessary. Small effective population size, low genetic diversity, and k-selected life history traits make these isolated populations vulnerable to region-specific anthropogenic threats, which include entanglement, boat strikes, and habitat degradation. The long-term persistence of reef manta rays in the Hawaiian Islands will require island-specific management strategies.
... Baiz et al., 2019;Combs et al., 2018;de Jong et al., 2020;Farleigh et al., 2021; Fritz et al., 2018;Ivanov et al., 2018;Maigret et al., 2020;Portnoy et al., 2015;Ryan et al., 2017;Schley et al., 2020;Termignoni- García et al., 2017;Trense et al., 2021) where size-selection was carried out using Pippin Prep or BluePippin before the PCR step. ...
Full-text available
Double‐digest Restriction‐site Associated DNA sequencing (ddRADseq) is widely used to generate genomic data for non‐model organisms in evolutionary and ecological studies. Along with affordable paired‐end sequencing, this method makes population genomic analyses more accessible. However, multiple factors should be considered when designing a ddRADseq experiment, which can be challenging for new users. The generated data often suffer from substantial read overlaps and adaptor contamination, severely reducing sequencing efficiency and affecting data quality. Here, we analyse diverse datasets from the literature and carry out controlled experiments to understand the effects of enzyme choice and size selection on sequencing efficiency. The empirical data reveal that size selection is imprecise and has limited efficacy. In certain scenarios, a substantial proportion of short fragments pass below the lower size‐selection cut‐off resulting in low sequencing efficiency. However, enzyme choice can considerably mitigate inadvertent inclusion of these shorter fragments. A simple model based on these experiments is implemented to predict the number of genomic fragments generated after digestion and size selection, number of SNPs genotyped, number of samples that can be multiplexed and the expected sequencing efficiency. We developed ddgRADer – – a user‐friendly webtool and incorporated these calculations to aid in ddRADseq experimental design while optimizing sequencing efficiency. This tool can also be used for single enzyme protocols such as Genotyping‐by‐Sequencing. Given user‐defined study goals, ddgRADer recommends enzyme pairs and allows users to compare and choose enzymes and size‐selection criteria. ddgRADer improves the accessibility and ease of designing ddRADseq experiments and increases the probability of success of the first population genomic study conducted in labs with no prior experience in genomics.
... Philopatric behavior of female sharks contributes to reduce connectivity among populations (already isolated in the context of oceanic islands in French Polynesia) where intrinsic reproduction and recruitment become the determinants of population dynamics 23 . Philopatry in sharks is a double-edged sword likely increasing the adaptation across heterogenous environments, the fitness by providing predictable access to food and shelter from predators but limiting the gene-flow because of the isolated oceanic islands context 10,24 . Moorea is a Polynesian island that has different types of ecosystems along its coastline including mangroves, sandflats, and coral reefs, which may influence the population dynamics of the local shark populations as sharks show complex habitat use patterns 3 . ...
Full-text available
The exploitation of sharks and the degradation of their habitats elevate the urgency to understand the factors that influence offspring survival and ultimately shark reproductive success. We monitored and sampled blacktip reef sharks (Carcharhinus melanopterus) in nursery habitats of Moorea Island (French Polynesia), to improve knowledge on shark reproductive behavior and biology. We sampled fin clips and morphometrics from 230 young-of-the-year sharks and used microsatellite DNA markers to process parentage analysis to study the reproductive philopatric behavior in female sharks and the matrotrophy within litters. These traits are driving the success of the local replenishment influencing selection through birth site and maternal reserves transmitted to pups. Parentage analysis revealed that some female sharks changed their parturition areas (inter-seasonally) while other female sharks came back to the same site for parturition, providing evidence for a plastic philopatric behavior. Morphometrics showed that there was no significant relationship between body condition indices and nursery locations. However, similarities and differences in body condition were observed between individuals sharing the same mother, indicating that resource allocation within some shark litters might be unbalanced. Our findings further our understanding of the reproductive biology and behavior that shape shark populations with the aim to introduce these parameters into future conservation strategies.
... However, when compared to the Atlantic population, studies of population genetics in NEP white sharks that have evaluated patterns in a mitochondrial genetic structure are scarce (uniparental molecular markers; Jorgensen et al. 2010, Oñate-González et al. 2015, Díaz-Jaimes et al. 2016, Santana-Morales et al. 2020, and limited information on the patterns of nuclear genetic structure (biparental molecular markers) is available (Bernard et al. 2018). This is particularly important because differences between maternally inherited mitochondrial markers and biparental loci have been used to evaluate sex-biased dispersal and female philopatry in many shark species (Schrey & Heist 2003, Karl et al. 2011, Daly-Engel et al. 2012, Portnoy et al. 2015, Sandoval-Castillo & Beheregaray 2015, Momigliano et al. 2017, Day et al. 2019, including white sharks from the Atlantic, the western Pacific, and South Africa (Pardini et al. 2001, Blower et al. 2012, O'Leary et al. 2015. Further, the lack of genetic diversity information for populations based on multiple molecular markers is problematic given that international conservation policies for highly migratory species, such as the white shark, must include the protection of genetic diversity at the population level to safeguard the survival of these species (Domingues et al. 2018, Huveneers et al. 2018. ...
Full-text available
The Northeastern Pacific (NEP) population of white sharks (Carcharodon carcharias) is genetically distinct from the rest of the world. This uniqueness results from adult fidelity to central California and Guadalupe Island aggregations sites. The strong mitochondrial genetic structure between the white sharks of central California and Guadalupe Island is also present, which indicates female philopatry. To date, few studies using nuclear DNA have found evidence of genetic patterns in the NEP white shark population, which could indicate that these sharks exhibit sex-biased dispersal. In this study, we evaluated the genetic structure, connectivity, and genetic diversity of NEP white sharks using samples from the southern California Bight (SCB), Baja California (including Sebastian Vizcaino Bay), the Gulf of California, and Guadalupe Island (GI) using nDNA (i.e. microsatellite loci). A total of five loci were successfully genotyped in 54 individuals. The patterns found in this study indicated low levels of genetic diversity among all localities (observed heterozygosity: Ho = 0.47), likely due to a founder effect. A slight genetic structure was present for NEP localities in this study (FST = 0.045, P = 0.0001), mainly identified between the SCB and GI locations. A sibship assignment analysis indicated low and moderate probabilities of full-and half-siblings between white shark juveniles from coastal areas, suggesting a high degree of connectivity between nursery areas in the NEP. Our results suggest that juveniles can mask the genetic structure in coastal zones.
... Differences found between bonnetheads from the eastern GOM include size at age, growth rate, and size and age at maturity (Parsons 1993a, b;Carlson and Parsons 1997;Lombardi-Carlson et al. 2003). In addition, studies in both the Atlantic and eastern GOM have shown site fidelity by adult bonnetheads (both sexes) to specific estuaries or bays during the summer months, on inter-and intra-annual time scales (Heupel et al. 2006;Driggers et al. 2014), results supported by Portnoy et al. (2015) using genomic techniques. Further, results of tag-recapture and acoustic monitoring in the eastern GOM indicate that individuals in some locations may remain resident for large portions of the year (Heupel et al. 2006). ...
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The age, growth, and maturity of bonnetheads, Sphyrna tiburo, inhabiting estuarine and coastal waters of the U.S. Gulf of Mexico (GOM) were investigated. Based on results of a concurrent population genetics study, two populations were examined, the eastern GOM and western GOM. Vertebrae were collected and aged from 1081 females and 811 males ranging in size 261–1060 mm and 227–898 mm fork length (FL), respectively. The von Bertalanffy growth model provided the best fit to length-at-age data. Eastern GOM von Bertalanffy parameters (length parameters in mm FL) were L∞ = 844, k = 0.23, to = -1.99, and Lo = 310 for females and L∞ = 680, k = 0.39, to = -1.44, and Lo = 294 for males. Western GOM von Bertalanffy parameters were L∞ = 1005, k = 0.20, to = -1.81, and Lo = 298 for females and L∞ = 807, k = 0.30, to = -1.44, and Lo = 285 for males. Maximum observed age was similar between populations with an overall maximum of 17.1 years for females, and 12.1 years for males. Length and age at 50% maturity for the eastern GOM was 661.5 mm and 4.9 years for females, and 564.1 mm and 3.5 years for males and for the western GOM 772.7 mm and 5.3 years for females, and 644.9 mm and 4.4 years for males. Bonnetheads in the eastern GOM generally grow faster and to smaller asymptotic lengths than those from the western GOM; however, longevity is similar between the two populations.
... Parturition is indicated to occur between December and January in the Indian Ocean, after a gestation period of 12 months, which is consistent with a mating season around this time of the year (Bass et al. 1973;Stevens 1984). The increased mobility of adult silvertip sharks in November-December in our study provides further support for the existence of a summer mating season, and may also explain the reduced detections of tagged silvertip sharks within a receiver array on the Great Barrier Reef between September and January (Espinoza et al. 2015b).Our results also suggest female philopatry and male-biased dispersal for both species, a strategy common to many shark species Portnoy et al. 2015), where males assume the function of dispersing genes across large spatial scales. While bringing new insight on the movements of the silvertip shark, a poorly documented species, our results also provide valuable information to inform protection measures. ...
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The silvertip shark, Carcharhinus albimarginatus, is a coral reef-associated shark with a wide distribution across the Indo-Pacific. Yet, unlike common reef shark species, limited knowledge exists on its movement patterns. Here, we tracked 28 individuals for 4 years with acoustic telemetry in New Caledonia to estimate home range sizes and to investigate individual and seasonal patterns of space use. Comparisons were made with grey reef sharks, C. amblyrhynchos, a closely related but more documented species, tagged on the same acoustic network during the same period. We report similar home range (HR) for both species, with adult males displaying greater HR than females and juveniles. An increased mobility of adult males was observed during the austral summer for the silvertip shark, and the austral winter for the grey reef shark, corresponding to putative mating seasons. Our study brings new insight on the ecology of the silvertip shark and provides essential material to inform targeted conservation measures.
The blue shark Prionace glauca and the shortfin mako Isurus oxyrinchus are two large and highly migratory sharks inhabiting temperate and tropical waters worldwide that are heavily targeted by artisanal and industrial fisheries. The International Union for Nature Conservation classifies the blue shark and shortfin mako as ‘Near Threatened’ and ‘Vulnerable’, respectively, in the Nature Red List of Threatened Species v. 2019‐2. This study examined the population genetics of the shortfin mako and blue sharks at a regional (south‐eastern Pacific Ocean) and global scale. The null hypothesis of no genetic discontinuities among ocean basins and/or between hemispheres was tested using two mitochondrial markers suitable for population genetics inference in these species: the non‐coding control region and the protein‐coding gene cytochrome c oxidase I in I. oxyrinchus , and the control region and cytochrome b in P. glauca . Spatial genetic analyses suggested a single and two genetic clusters co‐occurring along the south‐eastern Pacific Ocean in the shortfin mako and blue shark, respectively. Phylogeographic analyses, migration estimates, haplotype networks and AMOVAs demonstrated that the two species exhibit an overall pattern of high genetic connectivity among hemispheres and across ocean basins with a signature of shallow genetic structuring worldwide. This study has generated valuable information for the management and conservation of heavily exploited sharks and highlights the need for additional inclusive research programmes assessing inter‐regional genomic discontinuities using more statistically powerful genetic markers to determine with precision population genetic discontinuities (if any) in these and other highly migratory sharks.
Acipenseriformes (sturgeons and paddlefishes) are of substantial conservation concern, and development of genomic resources for these species is difficult due to past whole genome duplication. Development of disomic markers for polyploid organisms can be challenging due to difficulty in resolving alleles at a single locus from those among duplicated loci. In this study, we detail the development of disomic markers for the endangered pallid sturgeon (Scaphirhynchus albus) found in North America. One of the strategies for pallid sturgeon conservation is to stock U.S. rivers with offspring of pure pallid sturgeon, but introgression with the sympatric shovelnose sturgeon (S. platorynchus) threatens pallid sturgeon genetic integrity. Currently, 19 microsatellite loci are used to differentiate between both species and their hybrids, but the markers are insufficient to robustly identify backcrosses. We performed double digest restriction site-associated DNA sequencing (ddRADseq) on shovelnose sturgeon haploid gynogens to produce a reduced-representation genomic reference. Contiguous sequences that were heterozygous within a haploid individual were flagged as potentially encompassing multiple loci. Approximately 60 individuals of each species from two management units were sequenced, and reads were mapped to the haploid reference to identify single nucleotide polymorphisms (SNPs) at individual loci. The final dataset contained 11,082 microhaplotyped loci which offer at least an order of magnitude greater resolution for species discrimination than the current panel of 19 microsatellites. These markers will be used to examine a larger sample of Scaphirhynchus individuals throughout their ranges to determine the extent and trajectory of hybridization.
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Recently, the adaptive significance of maternal effects has been increasingly recognized. No longer are maternal effects relegated as simple `troublesome sources of environmental resemblance' that confound our ability to estimate accurately the genetic basis of traits of interest. Rather, it has become evident that many maternal effects have been shaped by the action of natural selection to act as a mechanism for adaptive phenotypic response to environmental heterogeneity. Consequently, maternal experience is translated into variation in offspring fitness.
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Population genomics has the potential to improve studies of evolutionary genetics, molecular ecology and conservation biology, by facilitating the identification of adaptive molecular variation and by improving the estimation of important parameters such as population size, migration rates and phylogenetic relationships. There has been much excitement in the recent literature about the identification of adaptive molecular variation using the population-genomic approach. However, the most useful contribution of the genomics model to population genetics will be improving inferences about population demography and evolutionary history.
The common approach to the multiplicity problem calls for controlling the familywise error rate (FWER). This approach, though, has faults, and we point out a few. A different approach to problems of multiple significance testing is presented. It calls for controlling the expected proportion of falsely rejected hypotheses — the false discovery rate. This error rate is equivalent to the FWER when all hypotheses are true but is smaller otherwise. Therefore, in problems where the control of the false discovery rate rather than that of the FWER is desired, there is potential for a gain in power. A simple sequential Bonferronitype procedure is proved to control the false discovery rate for independent test statistics, and a simulation study shows that the gain in power is substantial. The use of the new procedure and the appropriateness of the criterion are illustrated with examples.
Preface. Part I: Background: 1. Introduction. Why Employ Molecular Genetic Markers? Why Not Employ Molecular Genetic Markers? 2. History of Molecular Phylogenetics. Debates and Diversions from Molecular Systematics. Molecular Phylogenetics. 3. Molecular Tools. Protein Assays. DNA Assays. References to Laboratory Protocols. 4. Interpretative Tools. Categorical Subdivisions of Molecular Genetic Data. Molecular Clocks. Procedures for Phylogeny Reconstruction. Gene Trees versus Species Trees. Part II: Applications: 5. Individuality and Parentage. Genetic Identity versus Non-Identity. Parentage. 6. Kinship and Intraspecific Phylogeny. Close Kinship and Family Structure. Geographic Population Structure and Gene Flow. Phylogeography. Microtemporal Phylogeny. 7. Speciation and Hybridization. The Speciation Process. Hybridization and Introgression. 8. Species Phylogenies and Macroevolution. Rationales for Phylogeny Estimation. Special Approaches to Phylogeny Estimation. Prospectus for a Global Phylogeny. Special Topics in Molecular Phylogenetics. 9. Conservation Genetics. Issues of Heterozygosity. Issues of Phylogeny. Literature Cited. Index to Taxonomic Genera. General Index.