Less can be more: loss of MHC functional diversity can reflect adaptation to novel conditions during fish invasions

Abstract

The ability of invasive species to adapt to novel conditions depends on population size and environmental mismatch, but also on genetic variation. Away from their native range, invasive species confronted with novel selective pressures may display different levels of neutral versus functional genetic variation. However, the majority of invasion studies have only examined genetic variation at neutral markers, which may reveal little about how invaders adapt to novel environments. Salmonids are good model systems to examine adaptation to novel pressures because they have been translocated all over the world and represent major threats to freshwater biodiversity in the Southern Hemisphere, where they have become invasive. We examined patterns of genetic differentiation at seven putatively neutral (microsatellites) loci and one immune-related major histocompatibility complex (MHC class II-β) locus among introduced rainbow trout living in captivity (farmed) or under natural conditions (naturalized) in Chilean Patagonia. A significant positive association was found between differentiation at neutral and functional markers, highlighting the role of neutral evolutionary forces in shaping genetic variation at immune-related genes in salmonids. However, functional (MHC) genetic diversity (but not microsatellite diversity) decreased with time spent in the wild since introduction, suggesting that there was selection against alleles associated with captive rearing of donor populations that do not provide an advantage in the wild. Thus, although high genetic diversity may initially enhance fitness in translocated populations, it does not necessarily reflect invasion success, as adaptation to novel conditions may result in rapid loss of functional MHC diversity.

Keywords: Aquaculture escapes; Oncorhynchus mykiss; biological invasions; rainbow trout; rapid evolution; selection.

Figure 1

Sampling locations of rainbow trout (Oncorhynchus mykiss) populations in Chile. Free-living and farm populations are represented by open and closed circles, respectively. Each pie chart represents the proportion of escapees (black), hybrids (gray), and naturalized (white) trout across the 10 free-living populations. Map created using Maptool (http://www.seaturtle.org/maptool).

Figure 2

Relationship between MHC class II-β allelic richness (AR). Open and closed circles represent free-living and farm populations, respectively.

Figure 3

Allelic richness curves (AR; A) and 95% CI estimated using PAST for farmed, escapees, hybrids, and naturalized rainbow trout.

Figure 4

Frequency distribution of MHC class II-β alleles in farmed trout (black), recent escapees (dark gray), hybrids (light gray), and naturalized fish (white). Only the most discriminating alleles are shown (threshold value = 50%). All pairwise comparisons were significantly different except between hybrids and escapees and between hybrids and naturalized fish.