A quarter-million-year-old polymorphism drives reproductive mode variation in the pea aphid

Rimbault, M.; Legeai, F.; Peccoud, J.; Mieuzet, L.; Call, E.; Nouhaud, P.; Defendini, H.; Maheo, F.; Marande, W.; Theron, N.; Tagu, D.; Le Trionnaire, G.; Simon, J.-C.; Jaquiery, J.

doi:10.1101/2022.10.24.513443

bioRxiv · 10.1101/2022.10.24.513443

A quarter-million-year-old polymorphism drives reproductive mode variation in the pea aphid

Rimbault, M.·Legeai, F.·Peccoud, J.·Mieuzet, L.·Call, E.·Nouhaud, P.·Defendini, H.·Maheo, F.·Marande, W.·Theron, N.·Tagu, D.·Le Trionnaire, G.·Simon, J.-C.·Jaquiery, J.

View original source ↗Export metadata ↓

Abstract

Although asexual linages evolved from sexual lineages in many different taxa, the genetics of sex loss remains poorly understood. We addressed this issue in the pea aphid Acyrthosiphon pisum, whose natural populations encompass lineages performing cyclical parthenogenesis (CP) and producing one sexual generation per year, as well as obligate parthenogenetic (OP) lineages that can no longer produce sexual females but can still produce males. A SNP-based, whole-genome scan of CP and OP populations sequenced in pools (103 individuals from six populations) showed that a single X-linked region controls the variation in reproductive mode. This 840-kb region is highly divergent between CP and OP populations (FST = 34.9%), with >2000 SNPs or short Indels showing a high degree of association with the phenotypic trait. Comparison of de novo genome assemblies built from long reads did not reveal large structural rearrangements between CP and OP lineages within the candidate region. This reproductive polymorphism still appears relatively ancient, as we estimated its age at ~0.25 million years from the divergence between cp and op alleles. The low genetic differentiation between CP and OP populations at the rest of the genome (FST = 2.4%) suggests gene flow between them. Males from OP lineages thus likely transmit their op allele to new genomic backgrounds. This "contagious asexuality", combined with environment-induced selection (each reproductive mode being favored under different climates) probably contributes to the long-term persistence of the cp and op alleles. SignificanceAsexual taxa occur in all major clades of Eukaryotes and derive from related sexual species. Yet, the genetic basis for these transitions is poorly known because crosses cannot generally be performed to genetically map the ability to propagate asexually. As a result, only one gene responsible for sex loss has been identified in one animal species. Here, using pooled genome sequencing, we identified an 840kb region (carrying 32 genes) that controls the transition to permanent asexuality in the pea aphid. We also revealed that sexual and asexual alleles diverged 0.25 million years ago and that asexual lineages likely persist through contagious asexuality, providing new insights into the mechanisms of coexistence of sexual and asexual lineages.

Explore related subjects

evolutionary biology Preprint

Keep this discovery

Explore connections, maps & timelines

BibTeX RIS

Rimbault, M., Legeai, F., Peccoud, J., Mieuzet, L., Call, E., Nouhaud, P., Defendini, H., Maheo, F., Marande, W., Theron, N., Tagu, D., Le Trionnaire, G., Simon, J.-C., Jaquiery, J.. 2022-10-24. A quarter-million-year-old polymorphism drives reproductive mode variation in the pea aphid. https://doi.org/10.1101/2022.10.24.513443

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

bioRxiv2026

Ocean current models predict spatial structure for coastal biodiversity

Genomic diversity provides the raw material through which all evolutionary processes occur. Accurately describing how environmental features affect patterns of diversity shows promise in predicting the resilience of populations and entire communities to dynamic environments and novel stressors. Identifying the contribution of purely neutral responses to environmental effects can be difficult, especially across large spatial ranges with many covarying environmental features. Using an individual-based model of larvae carried by ocean currents, we predict patterns of neutral genomic diversity in a passively dispersed coastal species, suggesting large geographic regions of relative homogeneity with ancestry determined by the nearest "upstream" population with limited larval input. The genomic identity that dominates each region sharply transitions at the next such interruption, generating hierarchical structure and violating assumptions of isolation-by-distance. We call these upstream populations "lineage source regions" (LSRs), and we find strong concordance between LSR model predictions and an empirical population genomic survey of a keystone salt marsh mussel (Geukensia demissa). We quantitatively validate model performance and goodness-of-fit, updating baseline predictions of genomic diversity patterns from the classic isolation-by-distance model to this LSR framework. This spatially explicit coastal ancestry model has potential for generalization across passive dispersing species.

evolutionary biology↗

bioRxiv2026

TaxaAudit: A statistical model of consensus in phylogenetics identifies non-monophyletic taxa

Interpreting variation in genes and traits across species requires understanding their evolutionary relationships. Taxonomic hierarchies provide a practical approximation of the tree of life, with the NCBI taxonomy linking this framework directly to public sequence data. Some named groups, however, are not evolutionary clades, and recognizing these exceptions requires knowledge scattered across the phylogenetics literature. Here we introduce TaxaAudit, a statistical model that identifies taxonomic groups whose monophyly is repeatedly contradicted by published phylogenies. The model accounts for background taxonomic conflict and the ability of each study's species sampling to expose non-monophyly. Applied to 5,865 molecular phylogenies from TimeTree, TaxaAudit flagged 516 NCBI taxa at family rank and below for significant recurrent contradiction of monophyly. Excluding these taxa's monophyly requirements improved the taxonomy's agreement with independent phylogenomic reference trees and phylogenies withheld from discovery. Flagged taxa were also 3.61 times as likely as matched controls to have their monophyly challenged in publications outside the discovery set. In tree-inference experiments, excluding these monophyly constraints improved agreement with reference phylogenies relative to enforcing the unmodified taxonomy. By identifying groups whose monophyly should not be assumed, TaxaAudit lets researchers draw on published phylogenetic knowledge without reviewing the specialist literature for every taxon. This supports broader use of the NCBI taxonomy as an evolutionary framework for biological comparisons.

evolutionary biology↗

bioRxiv2026

Shared landscape, divergent genomes: Comparative population genomics of co-occurring flora in an isolated Australian mountain range

Understanding how landscape heterogeneity shapes genomic variation is key to conserving biodiversity and evolutionary potential. Yet conservation genomics is typically conducted at the single species level, limiting our ability to identify shared genomic patterns or understand how co-occurring taxa differ in their response to common environmental gradients. We assessed spatial patterns of genomic variation and their associations with geographic and environmental features among populations of nine co-existing plant species with contrasting life-histories and ecological traits across Gariwerd, a threatened biodiversity hotspot in south-eastern Australia. All species exhibited weak overall genetic structure, although the magnitude and spatial distribution of differentiation varied among species. Despite this variation, broadly consistent spatial trends were apparent, with higher genomic divergence largely concentrated in central zones and higher genomic diversity localised in southern regions of the landscape. Significant associations between genetic differentiation and geographic distance were observed in three species, while another species showed associations with environmental distance. These findings demonstrate that coexisting species can show overlapping spatial patterns in genomic variation while differing markedly in their associations with geographic and environmental variation across the same landscape. This comparative approach provides a basis for spatial prioritisation and conservation planning, while highlighting the complex eco-evolutionary processes operating across heterogeneous landscapes.

evolutionary biology↗