RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic

Abstract

Genomic studies of invasive species can reveal both invasive pathways and functional differences underpinning patterns of colonization success. The European green crab (Carcinus maenas) was initially introduced to eastern North America nearly 200 years ago where it expanded northwards to eastern Nova Scotia. A subsequent invasion to Nova Scotia from a northern European source allowed further range expansion, providing a unique opportunity to study the invasion genomics of a species with multiple invasions. Here, we use restriction‐site‐associated DNA sequencing‐derived SNPs to explore fine‐scale genomewide differentiation between these two invasions. We identified 9137 loci from green crab sampled from 11 locations along eastern North America and compared spatial variation to mitochondrial COI sequence variation used previously to characterize these invasions. Overall spatial divergence among invasions was high (pairwise FST ~0.001 to 0.15) and spread across many loci, with a mean FST ~0.052 and 52% of loci examined characterized by FST values >0.05. The majority of the most divergent loci (i.e., outliers, ~1.2%) displayed latitudinal clines in allele frequency highlighting extensive genomic divergence among the invasions. Discriminant analysis of principal components (both neutral and outlier loci) clearly resolved the two invasions spatially and was highly correlated with mitochondrial divergence. Our results reveal extensive cryptic intraspecific genomic diversity associated with differing patterns of colonization success and demonstrates clear utility for genomic approaches to delineating the distribution and colonization success of aquatic invasive species.

Genomewide evidence of environmentally mediated secondary contact of European green crab (Carcinus maenas) lineages in eastern North America

“…Nonoutlier and outlier clinal loci yielded estimates of dispersal on similar orders of magnitude (~80–140 km/generation) and are similar to estimates reported by Grosholz (); Klassen and Locke () and Shanks et al. () for green crab, and are consistent with the high degree of genomewide divergence detected between ecotypes (Jeffery, DiBacco, Van Wyngaarden et al., ).…”

“…Based on physiological evidence from Tepolt and Somero (), we predict that seasonal temperature minima are limiting the range expansion of the invasive green crab ecotypes and that environmentally associated genomic regions will track a steep cline in temperature previously reported in Atlantic Canada. This work builds directly on previous studies highlighting the genomic differences (Jeffery, DiBacco, Van Wyngaarden et al., ; Tepolt & Palumbi, ) and subsequent hybridization of two independent waves of invasion (Darling, Tsai, Blakeslee, & Roman, ; Jeffery, DiBacco, Wringe et al., ) to better understand the environmental correlates of population specific invasion success and secondary contact in this species. Our results will provide insight into how secondary contact dynamics can be correlated with environmental heterogeneity potentially constraining the success of coastal marine invaders, and will help to understand and predict future range expansions and contractions of green crab ecotypes.…”

“…This method detects correlations between environmental variables and genotypic variation to reveal outliers, while controlling for population structure ( K ) and unmeasured environmental variables as latent factors. We set K = 2 based on the results of previous discriminant analyses of principal components (DAPC) and STRUCTURE (Pritchard, Stephens, & Donnelly, ) results (Jeffery, DiBacco, Van Wyngaarden et al., ; Jeffery, DiBacco, Wringe et al., ). LFMM was run with a burn‐in of 5,000 iterations and 15,000 Markov Chain Monte Carlo (MCMC) iterations which were replicated five times.…”

“…Green crab are highly tolerant of a wide range of temperatures and salinities, encompassing a 25°C range in sea surface temperatures in their native range and a range in salinity tolerance of 4–52‰ in adults (Klassen & Locke, ; Tepolt & Somero, ). At least two independent introductions of green crab have occurred since the 1800s (Audet et al., ; Blakeslee et al., ; Roman, ), resulting in the establishment of genetically distinct northern and southern ecotypes (Jeffery, DiBacco, Van Wyngaarden et al., ; Tepolt & Palumbi, ). These ecotypes correspond to northern and southern populations in the native range (Roman, ).…”

PMERGE: Computational filtering of paralogous sequences from RAD‐seq data

“…We validated the performance of PMERGE on an Atlantic salmon dataset (see Bradbury et al, 2015 and a green crab dataset (see Jeffery et al, 2017). For reference comparisons, polymorphic catalog loci consensus sequences were aligned to version ICSASG_v2 of the Atlantic salmon reference genome (Lien et al, 2016) and the Green crab reference (Hleap et al, in preparation) using BLASTN version 2.2.28 (Altschul, Gish, Miller, Myers, & Lipman, 1990) using restriction enzyme SbfI, and the resulting fragments were sequenced.…”