1 | INTRODUCTION
Gene flow from planktonic larval dispersal has the potential to maintain
genetic panmixia over large distances in the marine realm
(Shaklee
& Bentzen, 1998), although this potential is not always realized.
Possible causes of departures from panmixia include historical
biogeographic separation, physical oceanographic barriers, larval
behavior, sweepstakes reproductive success (SRS), and natural selection
(reviewed
in Hellberg, 2009). Disentangling these causes is challenging because
they can act synergistically. Thus, a genetic break formed by a
vicariant event could subsequently be maintained by selection
(Schneider-Broussard,
Felder, Chlan, & Neigel, 1998), or larval behavior could exploit
oceanographic features to limit dispersal
(Kingsford
et al., 2002). Sometimes it is possible to exclude mechanisms a priori,
thus in species with low fecundity SRS can be eliminated as the cause of
chaotic patchiness
(Cornwell,
Fisher, Morgan, & Neigel, 2016). More generally, distinctive patterns
of genetic population structure are considered signatures of specific
mechanisms
(Hellberg,
Burton, Neigel, & Palumbi, 2002). Extensive sampling is needed to
adequately characterize these patterns, which can appear at different
scales across time, space and life stage. Furthermore, numerous marker
loci are needed to detect and quantify the typically low levels of
population structure in marine populations
(Waples,
1998). With the above considerations in mind, we undertook a survey of
single nucleotide polymorphisms (SNPs) in the blue crab,Callinectes sapidus , an economically important, well-studied
species
(Kennedy
& Cronin, 2007).
The life cycle of the blue crab favors dispersal away from natal
habitats
(Epifanio,
2007). Females release planktonic larvae offshore where they are
transported by currents for 4-6 weeks. Megalopae (post-larvae) migrate
to coastal brackish water habitats where they settle and metamorphose
into juveniles. After mating, mature females migrate to offshore
spawning sites, sometimes travelling hundreds of kilometers
(Aguilar
et al., 2005;
Gelpi,
Fry, Condrey, Fleeger, & Dubois, 2013). Most surveys of genetic
variation in North American blue crabs have found no detectable genetic
differentiation
(Berthelemy-Okazaki
& Okazaki, 1997;
Lacerda
et al., 2016;
McMillen-Jackson
& Bert, 2004;
Yednock
& Neigel, 2014) or very little
(McMillen-Jackson,
Bert, & Steele, 1994;
Plough,
2017) over distances up to thousands of kilometers. In the surveys that
found slight differentiation, it was detected near the limits of their
statistical power
(discussed
in Yednock & Neigel, 2014), which suggests that additional genetic
structure is present at undetectable levels. A few studies have found
slight temporal or life-stage shifts in the genetic composition of blue
crab populations
(Feng,
Williams, & Place, 2017;
McMillen-Jackson
et al., 1994;
Yednock
& Neigel, 2014). Temporal shifts can cause chaotic genetic patchiness,
a pattern of fluctuating small-scale spatial variation first described
in limpets
(Johnson
& Black, 1982,
1984).
Kordos and Burton
(1993)
reported anomalously high levels of temporal and spatial differentiation
for allozyme loci in blue crabs from the coast of Texas. It is possible
that pronounced genetic structure such as they described develops
episodically or at specific locations in blue crab populations, but see
Sullivan and Neigel
(2017)
on the misidentification of specimens as a plausible explanation for
some of these anomalous findings.
The native range of C. sapidus is disjunct along the Atlantic
coast of the Americas and encompasses at least two distinct genetic
units. The northern portion of the range extends from Massachusetts in
the U.S. to Venezuela while the southern portion extends from Bahia,
Brazil to Mar del Plata in Argentina
(Santos
& D’Incao, 2004). Yednock and Neigel
(2014)
found that blue crabs from the northern Gulf of Mexico were genetically
different from those from Venezuela (FST for each
locus between 0.06 and 0.68) but not from Mexico. Rodrigues and
co-workers
(2017)
found two mitochondrial lineages in blue crabs, one in both portions of
the species’ range and the other exclusive to the southern portion. It
is likely that unintended sampling of multiple species ofCallinectes has been a source of error in blue crab ecological
and population genetic research, especially for studies that included
early life stages that are difficult to identify to species
(Sullivan
and Neigel, 2017).
Our sampling program was designed to be sensitive to both low levels of
genetic differentiation and episodic genetic structure. We sampled
individuals from multiple locations, time points, and life stages to
characterize patterns of genetic differentiation rather than simply test
for its presence. Some SNPs were in genes targeted for their presumed
functions. These criteria led us to a genotyping method, the Infinium
Assay (Illumina), which is seldom used for population genetics of
non-model organisms. We were able to use the Infinium assay because an
annotated transcriptome allowed us to identify SNPs in protein-coding
regions and a draft genome helped us locate and avoid introns.
Our findings support the main conclusions of most previous studies: we
detected little genetic population structure in blue crabs from the Gulf
of Mexico and North Atlantic. In addition, there was no evidence of SRS:
we found neither chaotic genetic patchiness or closely related
individuals. Overall, it appears that levels of gene flow are high among
North American blue crabs as expected from their biology. Although these
findings might appear unremarkable, they point to an opportunity to
observe the effects of natural selection on genetic structure against a
background that is relatively free of other structuring mechanisms. Here
we focus on detection of genetic differentiation in blue crabs and its
plausible causes, exclusive of natural selection.