Latitudinal trend in the reproductive mode of the pea aphid Acyrthosiphon pisum invading a wide climatic range

Abstract

The maintenance of sexuality is a puzzling phenomenon in evolutionary biology. Many universal hypotheses have been proposed to explain the prevalence of sex despite its costs, but it has been hypothesized that sex could be also retained by lineage‐specific mechanisms that would confer some short‐term advantage. Aphids are good models to study the maintenance of sex because they exhibit coexistence of both sexual and asexual populations within the same species and because they invade a large variety of ecosystems. Sex in aphids is thought to be maintained because only sexually produced eggs can persist in cold climates, but whether sex is obligate or facultative depending on climatic conditions remains to be elucidated. In this study, we have inferred the reproductive mode of introduced populations of the pea aphid Acyrthosiphon pisum in Chile along a climatic gradient using phenotypic assays and genetic‐based criteria to test the ecological short‐term advantage of sex in cold environments. Our results showed a latitudinal trend in the reproductive mode of Chilean pea aphid population from obligate parthenogenesis in the north to an intermediate life cycle producing both parthenogenetic and sexual progeny in the southernmost locality, where harsh winters are usual. These findings are congruent with the hypothesis of the ecological short‐term advantage of sex in aphids.

Rapid turnover of a pea aphid superclone mediated by thermal endurance in central Chile

“…96%, respectively). However, aphid MLGs were not comparable with the ones found by Peccoud et al [23] because of some distinctive microsatellite markers and a different capillary sequencer used for this work (see Material and Methods section in Martel et al [47]).…”

“…These findings suggest the coexistence of different clonal lineages, considering that the main transmission mechanism for the secondary symbionts in aphids is maternal inheritance and that the pea aphid population of central Chile has shown to be strictly asexual [23,46]. (iii) In a more recent work, Martel et al [47] found not only one but two different MLGs in the same latitudinal range (APG2 and APG3) but in quite different proportions (approx. 4% and approx.…”

“…B 291: 20232462 exclusion [62]. Thus, the lack of genetic diversity of the pea aphid in central Chile due to its strictly asexual reproductive mode in this area [23,47] could explain the rapid change in the genetic structure of this population in a decade by the replacement of the original superclone (APG2) by a genetically distant one (APG3; figure 1). Importantly, APG3 is quite divergent from the MLGs found by Peccoud et al…”

“…We compared the current two lineages of A. pisum populations on alfalfa with the dominant lineage found by Peccoud et al [23] using the same microsatellite markers and protocol. Considering that among the main environmental changes in central Chile over the last decade are the rise in mean summer temperatures and the increased prevalence and magnitude of summer heatwaves [39][40][41][42][43][44], we hypothesized that the unbalanced proportions of the two MLG recorded by Martel et al [47] could be attributable to differences in thermal response between lineages. Additionally, we assessed the presence/absence and the identity of the secondary endosymbionts in these two lineages, considering that some secondary endosymbionts can protect their host aphids from acute heat events [48,49].…”

Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

“…The lack of both recombination and independent assortment of heritable elements, will complicate efforts to pinpoint targets of selection, a problem extending to maternally inherited symbionts of such asexuals [ 108 ]. Pea aphids show a mixture of sexual and asexual reproduction throughout varying parts of their range, e.g., [ 109 ]. As such, portions of some populations may survive presumably mild winter seasons as asexual, parthenogenetic morphs, instead of overwintering as cold-tolerant eggs produced by matings between male and female sexual morphs.…”