Inversion frequencies and phenotypic effects are modulated by the environment: insights from a reciprocal transplant study in Coelopa frigida

Emma Berdan,Keith Larson,Maren Wellenreuther,Hanna Rosenquist

doi:10.1007/s10682-018-9960-5

Abstract

Understanding how environmental variation drives phenotypic diversification within species is a major objective in evolutionary biology. The seaweed fly Coelopa frigida provides an excellent model for the study of genetically driven phenotypes because it carries an α/β inversion polymorphism that affects body size. Coelopa frigida inhabits highly variable beds of decomposing seaweed on the coast in Scandinavia thus providing a suitable test ground to investigate the genetic effects of substrate on both the frequency of the inversion (directional selection) and on the phenotype (genotype × environment effects). Here we use a reciprocal transplant experiment to test the effect of the α/β inversion on body size traits and development time across four suitable natural breeding substrates from the clinal distribution. We show that while development time is unaffected by G × E effects, both the frequency of the inversion and the relative phenotypic effects of the inversion on body size differ between population × substrate combinations. This indicates that the environment modulates the fitness as well as the phenotypic effects of the inversion karyotypes. It further suggests that the inversion may have accumulated qualitatively different mutations in different populations that interact with the environment. Together our results are consistent with the idea that the inversion in C. frigida likely evolves via a combination of local mutation, G × E effects, and differential fitness of inversion karyotypes in heterogeneous environments.

Highlights

One of the central goals of evolutionary biology is to understand how organisms cope with environmental heterogeneity (Savolainen et al 2013)
If environmentally adaptive variants are chromosomally linked, either because they are found on chromosomal inversions or are in areas of low recombination, their selective coefficients act in an additive manner and they may be less likely to be lost via genetic drift and more likely to contribute to rapid adaptation (Kirkpatrick and Barton 2006)
Complex adaptations may be accomplished through the fixation of linked sets of adaptive variants (Yeaman 2013), often called supergenes, a case in which polygenic adaptation may be more accurately modeled with single-locus models (Schwander et al 2014)

Summary

Introduction

One of the central goals of evolutionary biology is to understand how organisms cope with environmental heterogeneity (Savolainen et al 2013). Clines hold a large attraction as natural Darwinian laboratories because they allow researchers to quantify the gradual effects of changing environments on genotype, phenotype, and the interaction between them (Endler 1977). These studies have shown that while many environmental tolerance traits that vary clinally are quantitative and polygenic (Wellenreuther and Hansson 2016), they can be located within chromosomal segments that segregate as a single locus (Tigano and Friesen 2016). Good examples come from Drosophila melanogaster where inversion polymorphisms produce latitudinally varying phenotypes for traits including heat and cold tolerance and body size (Reinhardt et al 2014; Schrider et al 2016) and wing mimicry polymorphisms found in Heliconius butterflies (Thompson and Jiggins 2014)

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