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

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

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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.

Original languageEnglish
Pages (from-to)2348-2366
Number of pages19
JournalMolecular Ecology
Volume31
Issue number8
DOIs
StatePublished - Apr 2022

Bibliographical note

Funding Information:
We thank members of the Linnen laboratory for assistance with collection and rearing of pine sawflies, and we thank Kim Vertacnik for providing data from an outgroup taxon. We also thank three anonymous reviewers for constructive feedback. This work was supported by the National Science Foundation (DEB‐CAREER‐1750946 and DEB‐1257739 to C.R.L); USDA‐NIFA predoctoral fellowship (2015‐67011‐22803 to R.K.B.); Portuguese National Science Foundation (“Fundação para a Ciência e a Tecnologia”—FCT; UIDB/00329/2020, individual grants CEECIND/02391/2017 and CEECINST/00032/2018/CP1523/CT0008 to V.C.S.); and by the EU H2020 programme (Marie Skłodowska‐Curie grant no. 799729 to V.C.S.). For computing resources, we thank the University of Kentucky Center for Computational Sciences and the Lipscomb High Performance Computing Cluster, as well as the INCD ( https://incd.pt/ ), access to which was funded through FCT Advanced Computing Projects (CPCA/A0/7303/2020 to V.C.S.).

Funding Information:
We thank members of the Linnen laboratory for assistance with collection and rearing of pine sawflies, and we thank Kim Vertacnik for providing data from an outgroup taxon. We also thank three anonymous reviewers for constructive feedback. This work was supported by the National Science Foundation (DEB-CAREER-1750946 and DEB-1257739 to C.R.L); USDA-NIFA predoctoral fellowship (2015-67011-22803 to R.K.B.); Portuguese National Science Foundation (?Funda??o para a Ci?ncia e a Tecnologia??FCT; UIDB/00329/2020, individual grants CEECIND/02391/2017 and CEECINST/00032/2018/CP1523/CT0008 to V.C.S.); and by the EU H2020 programme (Marie Sk?odowska-Curie grant no. 799729 to V.C.S.). For computing resources, we thank the University of Kentucky Center for Computational Sciences and the Lipscomb High Performance Computing Cluster, as well as the INCD (https://incd.pt/), access to which was funded through FCT Advanced Computing Projects (CPCA/A0/7303/2020 to V.C.S.).

Publisher Copyright:
© 2022 John Wiley & Sons Ltd.

Keywords

  • faster-X
  • gene flow
  • genomic differentiation
  • haplodiploidy
  • local adaptation
  • speciation

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

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