Genetic Control of Contagious Asexuality in the Pea Aphid

Citation: Jaquiery J, Stoeckel S, Larose C, Nouhaud P, Rispe C, et al. ( Genetic Control of Contagious Asexuality in the Pea Aphid Julie Jaquie ry 0 1 Solenn Stoeckel 0 1 Chloe Larose 0 1 Pierre Nouhaud 0 1 Claude Rispe 0 1 Lucie Mieuzet 0 1 Joe l Bonhomme 0 1 Fre de rique Mahe o 0 1 Fabrice Legeai 0 1 Jean-Pierre Gauthier 0 1 Nathalie Prunier-Leterme 0 1 Denis Tagu 0 1 Jean-Christophe Simon 0 1 Mark Kirkpatrick, University of Texas, United States of America 0 a Current address: University of Rennes I, CNRS UMR6553 EcoBio, Rennes, France b Current address: Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland c Current address: INRA, UMR1300 Biology, Epidemiology and Risk Analysis in animal health , CS40706, Nantes , France 1 1 INRA, UMR1349, Institute of Genetics, Environment and Plant Protection , Domaine de la Motte, Le Rheu , France , 2 INRIA Centre Rennes - Bretagne Atlantique, GenOuest, Campus de Beaulieu , Rennes , France 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. Competing Interests; The authors have declared that no competing interests exist - 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]. Cyclical parthenogenesis (CP) represents a mixed reproductive mode with an alternation of sexual reproduction and parthenogenesis, and is reported in many animal species [4]. The loss of the sexual phase in CP species - leading to permanently parthenogenetic taxa - have been shown to arise from diverse mechanisms, including microbial infection, hybridization, contagion via pre-existing parthenogenetic lineages or spontaneous mutations [59]. Nevertheless, 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. However 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 therefore the genetic basis of the loss of sexual reproduction. In the rare cases where it has been explored, genetic control of this trait has been shown to be rather simple, with the involvement of one to four loci, depending on the studied organisms [1015]. However, the precise location and underlying function of these genetic factors have not been elucidated. The ancestral life-cycle of aphids is cyclical parthenogenesis [16], which consists in an alternation of sexual and asexual generations. In spring and summer, CP lineages produce asexual Asexual lineages occur in most groups of organisms and arise from loss of sex in sexual species. Yet, the genomic bases of these transitions remain largely unknown. Here, 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. Also, our population genetic data indicated substantial gene exchange between these reproductively distinct lineages, potentially leading to the conversion of some sexual lineages into asexual ones in a contagious manner. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual lineages. females through apomictic parthenogenesis. In autumn, asexual females give birth to males and sexual females in response to photoperiodic cues (note that CP lineages can also produce asexual females to some extent [e.g. 17]). Sexual females are strict clones of their asexual mothers, while one of the two X chromosomes is randomly lost to generate males [17]. Eggs produced by sexual females are the only frost-resistant stage in the aphid cycle. Hence, a CP life cycle is required to survive in regions with cold winters. In addition, many aphid species also encompass OP lineages which are characterized by an altered response to sexinducing environmental cues as they produce only asexual females (although they often produce some males [18,19]). These lineages are thus cold-sensitive because of their inability to lay eggs. Yet, OP lineages are favoured in regions with mild winters where they have a major demographic advantage over CP lineages [20,21]. Accordingly, CP lineages dominate in cold areas and OP lineages in warmer regions, and both coexist in regions with fluctuating winter temperatures [1820]. Because male production by OP lineages is difficult to prove in the wild, it has been demonstrated in a single study which also showed that these males actually contribute to sexual reproduction with CP lineages [22,23]. While the switch from clonal to sexual reproduction in CP aphids is triggered by photoperiodic changes, the loss of sexual form production in OP aphids is genetically determined, changes in environmental conditions having little or no effect on their reproductive phenotype [10,19]. Here, we combined QTL and genome (...truncated)