The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population

Mark J. Hanemaaijer, Travis C. Collier, Allison Chang, Chloe C. Shott, Parker D. Houston, Hanno Schmidt, Bradley Main, Anthony J. Cornel, Yoosook Lee, Gregory C Lanzaro

Research output: Contribution to journalArticle

7 Scopus citations

Abstract

Animal species are able to acquire new genetic material via hybridization and subsequent introgression. However, little is known about how foreign genomic material is incorporated into a population over time and what genes are susceptible to introgression. Here, we follow the closely related mosquito sister species Anopheles coluzzii and Anopheles gambiae in a sympatric natural population in Mali at multiple time points spanning a period of 25 years. During this period, we observed the temporary breakdown of mating barriers, which allowed us to explore the fate of alleles that crossed the species boundary in a natural population. Whole genome sequencing of 74 individuals revealed introgression within only 34 genes (0.26% of total genes) from A. gambiae to A. coluzzii, the majority contained within a 4 Mb region on the 2L chromosome which includes the insecticide resistance gene (AGAP004707). We designed a genotyping assay to follow 25 of the 34 introgressed alleles over time and found that all A. gambiae alleles, except four, reached a frequency of 50% in the A. coluzzii population within 4 years (~50 generations) and increased to ~80% within 6 years (~75 generations). However, the frequency of all introgressed alleles, except three, decreased to ~60% in 2016. This suggests an ongoing process of purifying selection in the population against DNA of foreign ancestry, except for alleles that are under positive selection, resulting in a complex genomic landscape. This study shows that stable introgression is limited to only specific genes even within closely related species.

Original languageEnglish (US)
Pages (from-to)4978-4990
Number of pages13
JournalMolecular Ecology
Volume27
Issue number24
DOIs
StatePublished - Dec 1 2018

Keywords

  • Anopheles
  • evolution
  • gene flow
  • hybridization
  • Introgression
  • population genomics
  • selection

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

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    Hanemaaijer, M. J., Collier, T. C., Chang, A., Shott, C. C., Houston, P. D., Schmidt, H., Main, B., Cornel, A. J., Lee, Y., & Lanzaro, G. C. (2018). The fate of genes that cross species boundaries after a major hybridization event in a natural mosquito population. Molecular Ecology, 27(24), 4978-4990. https://doi.org/10.1111/mec.14947