Novel insights into symbiont population structure: Globe-trotting avian feather mites contradict the specialist–generalist variation hypothesis

Alix E. Matthews, Than J. Boves, Andrew D. Sweet, Elizabeth M. Ames, Lesley P. Bulluck, Erik I. Johnson, Matthew Johnson, Sara E. Lipshutz, Katie L. Percy, Douglas W. Raybuck, Wendy M. Schelsky, Christopher M. Tonra, Catherine B. Viverette, Asela J. Wijeratne

Research output: Contribution to journalArticlepeer-review

Abstract

Researchers often examine symbiont host specificity as a species-level pattern, but it can also be key to understanding processes occurring at the population level, which are not as well understood. The specialist–generalist variation hypothesis (SGVH) attempts to explain how host specificity influences population-level processes, stating that single-host symbionts (specialists) exhibit stronger population genetic structure than multi-host symbionts (generalists) because of fewer opportunities for dispersal and more restricted gene flow between populations. However, this hypothesis has not been tested in systems with highly mobile hosts, in which population connectivity may vary temporally and spatially. To address this gap, we tested the SGVH on proctophyllodid feather mites found on migratory warblers (family Parulidae) with contrasting host specificities, Amerodectes protonotaria (a host specialist of Protonotaria citrea) and A. ischyros (a host generalist of 17 parulid species). We used a pooled-sequencing approach and a novel workflow to analyse genetic variants obtained from whole genome data. Both mite species exhibited fairly weak population structure overall, and contrary to predictions of the SGVH, the generalist was more strongly structured than the specialist. These results may suggest that specialists disperse more freely among conspecifics, whereas generalists sort according to geography. Furthermore, our results may reflect an unexpected period for mite transmission – during the nonbreeding season of migratory hosts – as mite population structure more closely reflects the distributions of hosts during the nonbreeding season. Our findings alter our current understanding of feather mite biology and highlight the potential for studies to explore factors driving symbiont diversification at multiple evolutionary scales.

Original languageEnglish (US)
Pages (from-to)5260-5275
Number of pages16
JournalMolecular ecology
Volume32
Issue number19
DOIs
StatePublished - Oct 2023

Keywords

  • dispersal
  • gene flow
  • host specificity
  • population genomics
  • symbiosis

ASJC Scopus subject areas

  • Genetics
  • Ecology, Evolution, Behavior and Systematics

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