Examining the role of parasites in limiting unidirectional gene flow between lake and river sticklebacks.

Noémie I Erin,Martin Kalbe,Irene E Samonte,Tina Henrich,Daniel P Benesh,Per J Jakobsen,Christophe Eizaguirre

doi:10.1111/1365-2656.13080

Abstract

Parasites are important selective agents with the potential to limit gene flow between host populations by shaping local host immunocompetence. We report on a contact zone between lake and river three-spined sticklebacks (Gasterosteus aculeatus) that offers the ideal biogeographic setting to explore the role of parasite-mediated selection on reproductive isolation. A waterfall acts as a natural barrier and enforces unidirectional migration from the upstream river stickleback population to the downstream river and lake populations. We assessed population genetic structure and parasite communities over four years. In a set of controlled experimental infections, we compared parasite susceptibility of upstream and downstream fish by exposing laboratory-bred upstream river and lake fish, as well as hybrids, to two common lake parasite species: a generalist trematode parasite, Diplostomum pseudospathaceum, and a host-specific cestode, Schistocephalus solidus. We found consistent genetic differentiation between upstream and downstream populations across four sampling years, even though the downstream river consisted of ~10% first-generation migrants from the upstream population as detected by parentage analysis. Fish in the upstream population had lower genetic diversity and were strikingly devoid of macroparasites. Through experimental infections, we demonstrated that upstream fish and their hybrids had higher susceptibility to parasite infections than downstream fish. Despite this, naturally sampled upstream migrants were less infected than downstream residents. Thus, migrants coming from a parasite-free environment may enjoy an initial fitness advantage, but their descendants seem likely to suffer from higher parasite loads. Our results suggest that adaptation to distinct parasite communities can influence stickleback invasion success and may represent a barrier to gene flow, even between close and connected populations.

Highlights

Natural selection can foster rapid adaptive ecological divergence when different populations adapt to divergent resources or habitats (Rundle, 2000; Rundle & Nosil, 2005)
We demonstrated that upstream fish and their hybrids had higher susceptibility to parasite infections than downstream fish
Our results suggest that adaptation to distinct parasite communities can influence stickleback invasion success and may represent a barrier to gene flow, even between close and connected populations

Summary

| INTRODUCTION

Natural selection can foster rapid adaptive ecological divergence when different populations adapt to divergent resources or habitats (Rundle, 2000; Rundle & Nosil, 2005). Host immunocompetence, that is the ability to overcome or cope with potential parasite infections, may vary through local adaptation and influence the success of migrants in new habitats, shaping host dispersal patterns and gene flow (Schmid‐Hempel & Ebert, 2003). Lake and river stickleback populations experience different parasite pressures, which appears to reinforce reproductive barriers by decreasing migration success and gene flow between neighbouring populations (Eizaguirre et al, 2011; Feulner et al, 2015; Kaufmann et al, 2017; MacColl & Chapman, 2010; Reusch, Wegner, et al, 2001b; Scharsack, Kalbe, Harrod, & Rauch, 2007a). We tested whether (a) gene flow was occurring from upstream to downstream populations; (b) whether parasite communities differed across sites and were stable over time; and (c) whether the upstream population differed in its resistance to parasite infections

| MATERIALS AND METHODS

| DISCUSSION

Findings

| CONCLUSIONS