Balanced polymorphism fuels rapid selection in an invasive crab despite high gene flow and low genetic diversity

Abstract

Adaptation across environmental gradients has been demonstrated in numerous systems with extensive dispersal, despite high gene flow and consequently low genetic structure. The speed and mechanisms by which such adaptation occurs remain poorly resolved, but are critical to understanding species spread and persistence in a changing world. Here, we investigate these mechanisms in the European green crab Carcinus maenas, a globally distributed invader. We focus on a northwestern Pacific population that spread across >12 degrees of latitude in 10 years from a single source, following its introduction <35 years ago. Using six locations spanning >1500 km, we examine genetic structure using 9376 single nucleotide polymorphisms (SNPs). We find high connectivity among five locations, with significant structure between these locations and an enclosed lagoon with limited connectivity to the coast. Among the five highly connected locations, the only structure observed was a cline driven by a handful of SNPs strongly associated with latitude and winter temperature. These SNPs are almost exclusively found in a large cluster of genes in strong linkage disequilibrium that was previously identified as a candidate for cold tolerance adaptation in this species. This region may represent a balanced polymorphism that evolved to promote rapid adaptation in variable environments despite high gene flow, and which now contributes to successful invasion and spread in a novel environment. This research suggests an answer to the paradox of genetically depauperate yet successful invaders: populations may be able to adapt via a few variants of large effect despite low overall diversity.

Seascape genomics identify adaptive barriers correlated to tidal amplitude in the shore crabCarcinus maenas

“…While our data suggest that tidal amplitude plays a major role in both barriers, other environmental drivers could also contribute. Temperature has been shown to play an important role in shaping population differentiation in several crustaceans, such as in American lobster (Benestan et al, 2016) and northern shrimp (Jorde et al, 2015), and a genomic island has been identified in the shore crab which might be associated with rapid temperature adaptation (Tepolt et al, 2021; Tepolt & Palumbi, 2020). The geographical area assessed here is located in the middle of the native distribution of C .…”

Ready on arrival: Standing variation at a chromosomal inversion contributes to rapid adaptation in an invasive marine crab

“…In this issue of Molecular Ecology, Tepolt et al (2021) illustrate how the genetic architecture of adaptation and life history influence invasive success. A marvel of many invasive species is that they are incredibly successful despite evolutionary expectations that they will have low adaptive potential and suffer inbreeding depression due to initially small founding population sizes.…”

“…Determining the combinations of ecoevolutionary factors that permit this apparent "genetic paradox of invasions" is an ongoing endeavour of invasive species research. Tepolt et al (2021) study the European green crab in its invasive range on the North American west coast. Following a single introduction into California, this crab quickly spread across a wide latitude gradient, despite low diversity in the original founding population.…”

“…Five sites were “open” to the northeast Pacific Ocean, whereas one site, Seadrift Lagoon, was an enclosed lagoon isolated from the broader oceanographic processes circulating along the coast. Tepolt et al (2021) characterised genomic variation using transcriptome sequencing. Overall, genome‐wide differentiation among sites was very low ( F ST < 0.03).…”

“…Distribution of a putative chromosomal inversion polymorphism in the European green crab associated with clinal adaptation to temperature in its invasive North American west coast range. (a) Study sites in Tepolt et al (2021) and an illustration of a green crab. (b) Schematic representation of genetic structure in a chromosomal inversion captured on a principal component (PC) axis.…”