Transcriptome sequencing reveals both neutral and adaptive genome dynamics in a marine invader

Abstract

Species invasions cause significant ecological and economic damage, and genetic information is important to understanding and managing invasive species. In the ocean, many invasive species have high dispersal and gene flow, lowering the discriminatory power of traditional genetic approaches. High-throughput sequencing holds tremendous promise for increasing resolution and illuminating the relative contributions of selection and drift in marine invasion, but has not yet been used to compare the diversity and dynamics of a high-dispersal invader in its native and invaded ranges. We test a transcriptome-based approach in the European green crab (Carcinus maenas), a widespread invasive species with high gene flow and a well-known invasion history, in two native and five invasive populations. A panel of 10 809 transcriptome-derived nuclear SNPs identified significant population structure among highly bottlenecked invasive populations that were previously undifferentiated with traditional markers. Comparing the full data set and a subset of 9246 putatively neutral SNPs strongly suggested that non-neutral processes are the primary driver of population structure within the species' native range, while neutral processes appear to dominate in the invaded range. Non-neutral native range structure coincides with significant differences in intraspecific thermal tolerance, suggesting temperature as a potential selective agent. These results underline the importance of adaptation in shaping intraspecific differences even in high geneflow marine invasive species. They also demonstrate that high-throughput approaches have broad utility in determining neutral structure in recent invasions of such species. Together, neutral and non-neutral data derived from high-throughput approaches may increase the understanding of invasion dynamics in high-dispersal species.

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

“…This is consistent with the findings of Tepolt and Palumbi (2015) who suggest secondary contact as the dominant structuring force in the introduced range. The presence of two distinct groups of green crab has been consistently reported previously using mtDNA (Roman, 2006), microsatellites (Darling et al., 2014), and RNA‐seq SNPs (Tepolt & Palumbi, 2015).…”

“…This is consistent with the findings of Tepolt and Palumbi (2015) who suggest secondary contact as the dominant structuring force in the introduced range. The presence of two distinct groups of green crab has been consistently reported previously using mtDNA (Roman, 2006), microsatellites (Darling et al., 2014), and RNA‐seq SNPs (Tepolt & Palumbi, 2015). This broad structuring of the two independent invasions in turn mirrors the spatial structuring of the native European range and is likely maintained by environmental differences between the northern and southern regions (Roman, 2006).…”

“…This broad structuring of the two independent invasions in turn mirrors the spatial structuring of the native European range and is likely maintained by environmental differences between the northern and southern regions (Roman, 2006). Our spatial analysis did reveal that two locations (PLB and KJI) appear intermediate between the northern and southern clusters which may be indicative of admixture and hybridization (Darling et al., 2014; Tepolt & Palumbi, 2015). One of these locations, Placentia Bay, is characterized by heavy shipping traffic, and the introduction of a previously admixed population from the Scotian Shelf is likely being maintained at this site (Blakeslee et al., 2010).…”

“…The data presented here are consistent with previous descriptions of green crab invasion history (Darling et al., 2014; Tepolt & Palumbi, 2015), suggesting two groups with southern Nova Scotia acting as the (potentially transient) geographic divide between northern and southern populations. This location is consistent with an initial observation by Darling et al.…”

“…In their native range, green crab show distinct broadscale structuring of island populations (i.e., Faeroe Islands and Iceland) and northern and southern European populations (Roman & Palumbi, 2004) using COI sequence data and fine‐scale (~450 km) structuring has been reported using microsatellite loci (Pascoal et al., 2009). In North America, spatial structuring is driven by both range expansion (Pringle, Blakeslee, Byers, & Roman, 2011) and secondary contact among invasions (Blakeslee et al., 2010; Darling et al., 2014; Tepolt & Palumbi, 2015). However, a genomewide comparison (i.e., RAD‐seq) of fine‐scale spatial structuring on the east coast has been absent and is warranted to compare these independent invasions and characterize the full genetic diversity of populations along this part of their invasive range.…”