On the genetic architecture of rapidly adapting and convergent life history traits in guppies

Sophie Matthews,Josephine R Paris,James R Whiting,Paul J Parsons,David Reznick,Bonnie A Fraser,Kimberly A Hughes,Yuridia Reynoso

doi:10.1038/s41437-022-00512-6

Abstract

The genetic basis of traits shapes and constrains how adaptation proceeds in nature; rapid adaptation can proceed using stores of polygenic standing genetic variation or hard selective sweeps, and increasing polygenicity fuels genetic redundancy, reducing gene re-use (genetic convergence). Guppy life history traits evolve rapidly and convergently among natural high- and low-predation environments in northern Trinidad. This system has been studied extensively at the phenotypic level, but little is known about the underlying genetic architecture. Here, we use four independent F2 QTL crosses to examine the genetic basis of seven (five female, two male) guppy life history phenotypes and discuss how these genetic architectures may facilitate or constrain rapid adaptation and convergence. We use RAD-sequencing data (16,539 SNPs) from 370 male and 267 female F2 individuals. We perform linkage mapping, estimates of genome-wide and per-chromosome heritability (multi-locus associations), and QTL mapping (single-locus associations). Our results are consistent with architectures of many loci of small-effect for male age and size at maturity and female interbrood period. Male trait associations are clustered on specific chromosomes, but female interbrood period exhibits a weak genome-wide signal suggesting a potentially highly polygenic component. Offspring weight and female size at maturity are also associated with a single significant QTL each. These results suggest rapid, repeatable phenotypic evolution of guppies may be facilitated by polygenic trait architectures, but subsequent genetic redundancy may limit gene re-use across populations, in agreement with an absence of strong signatures of genetic convergence from recent analyses of wild guppies.

Highlights

IntroductionRecent evidence that phenotypes can evolve rapidly (Sanderson et al 2021) and often with surprising repeatability (convergence) (Waters and McCulloch 2021) has led to a re-evaluation of our expectations surrounding adaptation in nature
Using an F2 quantitative trait locus (QTL) breeding cross design, we examine the genetic basis of seven life history traits in guppies: female age (1) and size (2) at first brood, first brood size (3), interbrood period (4), average dry offspring weight in the first brood (5), and male age (6) and size (7) at maturity
Both male size and age at maturity, exhibit significant heritability associated with particular chromosomes, suggesting polygenic traits, but little evidence of genome-wide polygenicity or largeeffect loci

Summary

Introduction

Recent evidence that phenotypes can evolve rapidly (Sanderson et al 2021) and often with surprising repeatability (convergence) (Waters and McCulloch 2021) has led to a re-evaluation of our expectations surrounding adaptation in nature. The architecture of adaptive traits is predicted to moderate dependencies on the initial frequency of potentially adaptive alleles, as well as the size of the phenotypic response to selection, impacting population viability (Kardos and Luikart 2021). Empirical support for such predictions is important due to the current global circumstances of rapid environmental change, and to understand adaptation more generally. There are currently theoretical expectations surrounding which of these are most likely to underlie rapidly evolving (Pritchard et al 2010; Jain and Stephan 2017b) and/or convergent phenotypes (Yeaman et al.2018) but empirical evidence supporting these hypotheses is only starting to accumulate. We aim to elucidate the genetic architecture of a canonical example of convergent and rapid evolution using a quantitative genetics approach: life history traits in Trinidadian guppies

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