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).