Faster‐haplodiploid evolution under divergence‐with‐gene‐flow: Simulations and empirical data from pine‐feeding hymenopterans

Year: 2022

Type: article

Abstract: Although haplodiploidy is widespread in nature, the evolutionary consequences of this mode of reproduction are not well characterized. Here, we examine how genome-wide hemizygosity and a lack of recombination in haploid males affects genomic differentiation in populations that diverge via natural selection while experiencing gene flow. First, we simulated diploid and haplodiploid "genomes" (500-kb loci) evolving under an isolation-with-migration model with mutation, drift, selection, migration and recombination; and examined differentiation at neutral sites both tightly and loosely linked to a divergently selected site. As long as there is divergent selection and migration, sex-limited hemizygosity and recombination cause elevated differentiation (i.e., produce a "faster-haplodiploid effect") in haplodiploid populations relative to otherwise equivalent diploid populations, for both recessive and codominant mutations. Second, we used genome-wide single nucleotide polymorphism data to model divergence history and describe patterns of genomic differentiation between sympatric populations of Neodiprion lecontei and N. pinetum, a pair of pine sawfly species (order: Hymenoptera; family: Diprionidae) that are specialized on different pine hosts. These analyses support a history of continuous gene exchange throughout divergence and reveal a pattern of heterogeneous genomic differentiation that is consistent with divergent selection on many unlinked loci. Third, using simulations of haplodiploid and diploid populations evolving according to the estimated divergence history of N. lecontei and N. pinetum, we found that divergent selection would lead to higher differentiation in haplodiploids. Based on these results, we hypothesize that haplodiploids undergo divergence-with-gene-flow and sympatric speciation more readily than diploids.

Source: Molecular Ecology

DOI: 10.1111/mec.16410

Authors: Emily E. Bendall, Robin K. Bagley, Vitor C. Sousa, Catherine R. Linnen

Institutions: University of Kentucky, University of Michigan, The Ohio State University at Lima, University of Lisbon

Language: English

Topic: Genetic diversity and population structure

Subfield: Genetics

Field: Biochemistry, Genetics and Molecular Biology

Domain: Life Sciences

Open Access status: green

Funders: National Science Foundation, U.S. Department of Agriculture, European Commission, Universidade Nova de Lisboa, National Institute of Food and Agriculture, Horizon 2020 Framework Programme, Fundação para a Ciência e a Tecnologia, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, National Science Foundation of Sri Lanka, Division of Environmental Biology

OpenAlex ID: W3214438893