Drainage-structuring of ancestral variation and a common functional pathway shape limited genomic convergence in natural high- and low-predation guppies.

James R Whiting,Paul J Parsons,Bonnie A Fraser,Mijke J Van Der Zee,Detlef Weigel,Josephine R Paris,Mikkel H Schierup

doi:10.1371/journal.pgen.1009566

James R Whiting, Paul J Parsons + Show 5 more

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https://doi.org/10.1371/journal.pgen.1009566

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Abstract

Studies of convergence in wild populations have been instrumental in understanding adaptation by providing strong evidence for natural selection. At the genetic level, we are beginning to appreciate that the re-use of the same genes in adaptation occurs through different mechanisms and can be constrained by underlying trait architectures and demographic characteristics of natural populations. Here, we explore these processes in naturally adapted high- (HP) and low-predation (LP) populations of the Trinidadian guppy, Poecilia reticulata. As a model for phenotypic change this system provided some of the earliest evidence of rapid and repeatable evolution in vertebrates; the genetic basis of which has yet to be studied at the whole-genome level. We collected whole-genome sequencing data from ten populations (176 individuals) representing five independent HP-LP river pairs across the three main drainages in Northern Trinidad. We evaluate population structure, uncovering several LP bottlenecks and variable between-river introgression that can lead to constraints on the sharing of adaptive variation between populations. Consequently, we found limited selection on common genes or loci across all drainages. Using a pathway type analysis, however, we find evidence of repeated selection on different genes involved in cadherin signaling. Finally, we found a large repeatedly selected haplotype on chromosome 20 in three rivers from the same drainage. Taken together, despite limited sharing of adaptive variation among rivers, we found evidence of convergent evolution associated with HP-LP environments in pathways across divergent drainages and at a previously unreported candidate haplotype within a drainage.

Highlights

The process of adaptation in nature can be thought of as a complex interplay between random happenstance and repeatable processes in independent lineages
We establish expectations regarding how potentially adaptive genetic variation is distributed and shared among populations; informing on the most likely mode by which genetic convergence may occur in this system
We have investigated whether convergent HP-LP phenotypes that have evolved repeatedly within rivers across Northern Trinidad are underpinned by convergent genetic changes

Summary

Introduction

The process of adaptation in nature can be thought of as a complex interplay between random happenstance and repeatable processes in independent lineages The latter of these, often termed convergent or parallel evolution [1,2], has provided a myriad of examples from which general rules and principles of adaptation have been dissected under natural conditions. Stickleback adapting to freshwater experience selection on ancestral eda haplotypes [25] and de novo mutation at the pitx gene [10] to repeatedly evolve freshwater bony armour plate and pelvis phenotypes respectively. Pease et al [26] found all three modes of convergence occurring across a clade of wild tomato accessions: adaptive introgression of alleles associated with immunity to fungal pathogens, selection on an ancestral allele conferring fruit colour, and repeated de novo mutation of alleles associated with seasonality and heavy metal tolerance. The authors found glyphosate-resistance evolved in one location by introgression and selection on a pre-adapted allele, in another by the fixation of a shared ancestral haplotype, and in a third location through selection on multiple, derived haplotypes

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