Genetic control of contagious asexuality in the pea aphid.

Julie Jaquiéry,Solenn Stoeckel,Jean-Christophe Simon,Denis Tagu,Claude Rispe,Lucie Mieuzet,Chloé Larose,Joël Bonhomme,Jean-Pierre Gauthier,Nathalie Prunier-Leterme,Fabrice Legeai,Pierre Nouhaud,Frédérique Mahéo

doi:10.1371/journal.pgen.1004838

Abstract

Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.

Highlights

While sexuality is the dominant reproductive mode in metazoans, parthenogenesis - the development of an embryo from an unfertilized egg - occurs in most branches of the animal kingdom [e.g. 1,2,3]
We combined quantitative genetic and population genomic approaches to unravel the genetic control of shifts towards permanent asexuality in the pea aphid, which conveniently shows coexisting sexual and asexual lineages
We identified one main genomic region responsible for this transition located on the X chromosome

Summary

Introduction

While sexuality is the dominant reproductive mode in metazoans, parthenogenesis - the development of an embryo from an unfertilized egg - occurs in most branches of the animal kingdom (e.g. molluscs, insects, crustaceans, nematodes, fish, reptiles) [e.g. 1,2,3]. In case of contagious or mutational origin, the precise genomic regions responsible for the transitions to obligate parthenogenesis (OP) remain largely unknown, mostly because dissecting the genetic bases of that trait using recombination-based approaches is not possible in strictly asexual species. Several species show coexisting CP and OP lineages, with OP lineages often retaining a residual production of males. Such species offer ideal systems to decipher the heredity and the genetic basis of the loss of sexual reproduction. The precise location and underlying function of these genetic factors have not been elucidated

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Conclusion