INTRODUCTION
Understanding genetic diversity and connectivity between populations of
marine species is critical to inform the conservation and management of
the marine environment (Palumbi 2004; Baco et al. 2016; Xuereb et al.
2019). Historically, marine populations have been assumed to be
demographically open, owing to their large population sizes, high larval
dispersal potential and the perceived lack of physical barriers to gene
flow in the marine environment (Palumbi 1994; Waples 1998). However,
several studies have shown distinct patterns of population structure in
marine species, even at small spatial scales (e.g.,
Hoffman et al. 2011a; Benestan et
al. 2015; D’Aloia et al. 2015; DiBattista et al. 2017; Coscia et al.
2020), supporting the prospect of a seascape fragmented not only by
geographical barriers, but by environmental gradients (e.g., ocean
currents, tidal mixing fronts, temperature) that can act as either
conduits or barriers to dispersal (Galindo et al. 2006; Treml et al.
2015; Benestan et al. 2016).
The dispersal potential of marine invertebrates and hence gene flow
within and among populations is driven not only by the environment but
also by their life history strategy
(Shanks 2009; Selkoe & Toonen
2011). The majority of benthic marine invertebrates have a complex life
cycle with a planktonic larval phase (Thorson 1950). Larvae, especially
those with long planktonic life spans, are expected to disperse widely,
leading to high levels of gene flow. The relationship between pelagic
larval duration (PLD) and genetic connectivity, however, has been shown
to be weak in some cases (Weersing & Toonen 2009). Even in taxa without
larval stages (i.e., those with direct developing juveniles), there are
contradictory patterns. Whilst low levels of connectivity and hence gene
flow might be expected in such species (e.g.,
Sherman et al. 2008; Hoffman et
al. 2011b; Pascual et al. 2017), molecular studies have provided an
increasing number of exceptions to this assumption (e.g., Edmands &
Potts 1997; Kyle & Boulding 2000; Ayre & Hughes 2000; Richards 2007).
Beyond estimating genetic connectivity, genome-wide datasets facilitate
the characterization of the adaptive potential of populations. Further,
when aligned with spatial and environmental data, we can identify the
variables underlying the organization of adaptive genetic structure
(i.e., the seascape genomics framework; Selkoe et al. 2010, 2016; White
et al. 2010; Benestan et al. 2016; Bernatchez et al. 2019). Given that
marine species are generally characterised by large effective population
sizes (Ne ), and the efficacy of selection increases with
increasing Ne (via a reduction in genetic drift), marine
populations should be particularly well suited to exhibit local
adaptation (Allendorf et al. 2010; Gagnaire et al. 2015). The
theoretical expectation that selection is counteracted by the
homogenizing effects of gene flow (Lenormand 2002) suggests that
responses to selection may differ between species with different
propensities for gene flow. Specifically, species with more restricted
gene flow (i.e., direct developing species) may demonstrate stronger
effects of selection than species that disperse more widely (i.e.,
broadcast spawning species), in which locally adapted populations will
be swamped by the immigration of maladapted genotypes (e.g., Yamada
1989). Recent evidence, however, suggests that local adaptations can
persist in marine populations despite ongoing gene flow (Tigano &
Friesen 2016; Hoey & Pinsky 2018; Sandoval-Castillo et al. 2018; Teske
et al. 2019).
Here, we estimate the neutral and adaptive genetic structure of two
similarly distributed rocky intertidal gastropods (Nucella
lapillus and Steromphala umbilicalis ) in the Irish Sea using
restriction site-associated DNA (RADseq) datasets. S. umbilicalisis a broadcast spawning gastropod mollusc inhabiting mid- to
low-intertidal zones from Morocco (Southward et al. 1995) to north-west
Scotland (Mieszkowska et al. 2013).
It produces lecithotrophic larvae
with a maximum larval duration of 7-9 days (Keith et al. 2011). N.
lapillus is a gastropod mollusc of the low intertidal zone within the
north Atlantic (Wares & Cunningham 2001). It reproduces by
ovo-viviparity; fertilization is internal, egg capsules are laid on
rocky intertidal surfaces, and juvenile snails emerge after 8-12 weeks
(Strathmann 1987).
The combination of limited adult movement (e.g., up to 30 m; Castle &
Emery 1981) and direct development of juveniles leads to an expectation
of low gene flow and high differentiation in N. lapillus .
Although there has been some support for this (e.g., Rolán et al. 2004;
Bell & Okamura 2005), in many cases, evidence of higher gene flow has
emerged (e.g., Colson & Hughes 2007; Bell 2008). For example, Colson &
Hughes (2004) demonstrated levels of genetic differentiation in the
British Isles that were comparable to that of species with short-lived
pelagic larval reproduction. These results support rapid and common
medium-distance movements in N. lapillus (10-100 km), probably
through the passive transport of egg masses or small juveniles via
rafting. Further, clinal genetic differentiation over environmental
gradients, and genetic differentiation between morphs support the
contribution of heritable adaptive genetic differentiation to ecotypes
of N. lapillus (Kirby 2000;
Rolán et al. 2004; Guerra-Varela et al. 2009; Carro et al. 2019). While
less is known about the population structure of S. umbilicalis ,
Wort et al. (2019) showed no evidence of genetic differentiation between
populations separated by an ~230 km habitat gap,
suggesting that currents, PLD and spawning season are more important
than distance in determining genetic differentiation in this
species.
The rocky habitat required by our model species is linear and contains
long gaps formed by stretches of soft sediment or open sea. This allows
us to compare connectivity of a direct developing vs. a larval
dispersing species across habitat gaps using a combination of neutral
and adaptive genetic markers. With
regard to neutral genetic variation, we predict that the larval
dispersing S. umbilicalis will show greater connectivity across
large habitat gaps, whereas the direct developing N. lapilluswill show finer scale local structure. With regard to adaptive genetic
variation, we hypothesize that selection will overcome the homogenizing
effects of gene flow, resulting in more complex patterns of population
structure associated with the key environmental variables driving
selection in each species.
In addition to comparisons of genetic connectivity, we also estimate the
relative contribution of physical and environmental variables (spatial
structure, oceanography, climate) on patterns of neutral and adaptive
genetic structure in a seascape genomics framework. Provided that
oceanographic features are well represented by hydrodynamic model
simulations, their influence on dispersal and thus connectivity can be
estimated using larval dispersal algorithms that incorporate simulated
ocean flows with species biological traits (e.g., Robins et al. 2013).
Such methods can also be used to investigate stepping-stone dispersal
over successive generations (e.g., Giménez et al. 2020a). In addition to
oceanography, we investigate the influence of sea surface temperature
(SST) and air temperature (AT) on population structure, both of which
have been related to the distribution and abundance of our model species
(Southward & Crisp 1954; Kendall et al. 1987) and are important
selective agents driving population divergence in marine invertebrates
(Sanford & Kelly 2011). We also include wave exposure in our
environmental dataset, as it has been shown to affect the abundance ofS. umbilicalis (Ballantine 1961) and underlies the morphological
variation delineating ecotypes of N. lapillus (Guerra-Varela et
al. 2009; Carro et al. 2019).