Genotype-by-environment interactions drive the maintenance of genetic variation in a Salmo trutta L. hybrid zone.

Dorinda Marie Folio,Jordi Gil,Jacques Labonne,Arnaud Caudron

doi:10.1111/eva.13307

Abstract

Allopatric gene pools can evolve in different directions through adaptive and nonadaptive processes and are therefore a source of intraspecific diversity. The connection of these previously isolated gene pools through human intervention can lead to intraspecific diversity loss, through extirpation of native populations or hybridization. However, the mechanisms leading to these situations are not always explicitly documented and are thus rarely used to manage intraspecific diversity. In particular, genotype‐by‐environment (GxE) interactions can drive postzygotic reproductive isolation mechanisms that may result in a mosaic of diversity patterns, depending on the local environment. We test this hypothesis using a salmonid species (Salmo trutta) in the Mediterranean (MED) area, where intensive stocking from non‐native Atlantic (ATL) origins has led to various outcomes of hybridization with the native MED lineage, going from MED resilience to total extirpation via full hybridization. We investigate patterns of offspring survival at egg stage in natural environments, based on parental genotypes in interaction with river temperature, to detect potential GxE interactions. Our results show a strong influence of maternal GxE interaction on embryonic survival, mediated by maternal effect through egg size, and a weak influence of paternal GxE interaction. In particular, when egg size is large and temperature is cold, the survival rate of offspring originating from MED females is three times higher than that of ATL females’ offspring. Because river temperatures show contrast at small scale, this cold adaptation for MED females’ offspring constitutes a potent postzygotic mechanism to explain small‐scale spatial heterogeneity in diversity observed in MED areas where ATL fish have been stocked. It also indicates that management efforts could be specifically targeted at the environments that actively favor native intraspecific diversity through eco‐evolutionary processes such as postzygotic selection.

Highlights

Admixture of previously isolated gene pools, through human intervention, often leads to gene flow and hybridization
Among the 65 recovered boxes, some parent contributions could not be represented in some rivers, either due to nest scouring or to the lack of gametes and possibly reducing overall available genetic variation for selection
This study expands our knowledge of GxE interactions and reproductive isolation mechanisms between genetically distinct lineages brought in sympatry, by showing that fitness variation in hybrid zones following admixture can be strongly related to genetic origins and can be extremely spatially variable

Summary

| INTRODUCTION

Admixture of previously isolated gene pools, through human intervention, often leads to gene flow and hybridization. Information on the environmental factors that may contribute to reproductive isolation will help in understanding and predicting the outcomes of hybridization in specific environments This could be used to implement new management practices (Epifanio & Nielsen, 2001; Genovart, 2009; Todesco et al, 2016) to either avoid admixture (if applied soon enough), lesser the extent of introgression, and favor “native” genes conservation when admixture has already occurred (Caudron, Champigneulle, et al, 2012), or to favor diversity when it enhances the adaptive potential of the population (Chan et al, 2019). Based on our results and interpretation of GxE interactions, we propose new evolutionary-based guidelines for management strategies, to either enhance native diversity conservation or maintain adaptive potential in spatially variable environments

| MATERIALS AND METHODS

| RESULTS

| DISCUSSION