Adaptation to enemy shifts: rapid resistance evolution to local Vibrio spp. in invasive Pacific oysters

Abstract

One hypothesis for the success of invasive species is reduced pathogen burden, resulting from a release from infections or high immunological fitness of invaders. Despite strong selection exerted on the host, the evolutionary response of invaders to newly acquired pathogens has rarely been considered. The two independent and genetically distinct invasions of the Pacific oyster Crassostrea gigas into the North Sea represent an ideal model system to study fast evolutionary responses of invasive populations. By exposing both invasion sources to ubiquitous and phylogenetically diverse pathogens (Vibrio spp.), we demonstrate that within a few generations hosts adapted to newly encountered pathogen communities. However, local adaptation only became apparent in selective environments, i.e. at elevated temperatures reflecting patterns of disease outbreaks in natural populations. Resistance against sympatric and allopatric Vibrio spp. strains was dominantly inherited in crosses between both invasion sources, resulting in an overall higher resistance of admixed individuals than pure lines. Therefore, we suggest that a simple genetic resistance mechanism of the host is matched to a common virulence mechanism shared by local Vibrio strains. This combination might have facilitated a fast evolutionary response that can explain another dimension of why invasive species can be so successful in newly invaded ranges.

Additive transcriptomic variation associated with reproductive traits suggest local adaptation in a recently settled population of the Pacific oyster, Crassostrea gigas

“…So far, colonization of C. gigas on European coasts has been investigated by ecological or marker-based population genetic approaches, but the variability of phenotypic traits potentially associated with this range expansion has only very recently been investigated [7]. Despite strong difference in expression levels between sexes, as previously reported [53], we nonetheless detected a clear difference in expression levels between progenies of oysters originated from France and Denmark, and their hybrids.…”

“…However, by focusing on a population likely to have adapted to a new environment during invasion (Denmark), we have access to the adaptation filter on phenotypic evolution and uncover additively behaving traits (intermediate expression in hybrids) in the subset of transcripts that are the most differentially expressed. Interestingly, Wendling and Wegner [7] recently investigated the adaptive potential of North Sea C. gigas populations to local Vibrio spp., proposing that dominantly inherited resistance could facilitate fast adaptation. In our study, ANOVA and eP ST analyses gave complementary results on phenotypic traits differentiation between the Danish and the French progenies.…”

“…Invasive species are privileged models to analyse the evolution and adaptation of life history traits in new environments [1,2] While an increasing number of studies have documented adaptation during invasion in terrestrial species [3,4], few studies have been conducted in marine species to date [5][6][7]. Many marine species have a benthic sessile adult phase and disperse via a planktonic larval stage.…”

Parasites and marine invasions: Ecological and evolutionary perspectives

“…mass mortalities that are particularly common in the marine environment (Fey et al, 2015), but have only rarely led to research on associated evolutionary change (e.g. host adaptation: Wendling and Wegner, 2015;enemy release: Friedman et al, 2014).…”

Ecology and evolution of marine parasites and diseases: International NIOZ–AWI symposium, 10–14 March 2014, Texel, The Netherlands

“…One conceptual ecological framework that is already quite successfully integrated into marine parasitology is the study of biological invasions (Goedknegt et al, in press). Biological invasions offer an opportunity to investigate host-parasite interactions on the ecosystem scale, but can also be used to study evolutionary dynamics in natural systems (Goedknegt et al, 2015;Wendling and Wegner, 2015).…”