Semipermeable species boundaries create opportunities for gene flow and adaptive potential

Author:

Satokangas I.1ORCID,Nouhaud P.2ORCID,Seifert B.3ORCID,Punttila P.4ORCID,Schultz R.3ORCID,Jones M. M.5ORCID,Sirén J.5ORCID,Helanterä H.6ORCID,Kulmuni J.178ORCID

Affiliation:

1. Organismal & Evolutionary Biology Research Programme University of Helsinki Helsinki Finland

2. CBGP, INRAE, CIRAD, IRD, Montpellier SupAgro Univ Montpellier Montpellier France

3. Department of Entomology Senckenberg Museum für Naturkunde Görlitz Germany

4. Biodiversity Centre Finnish Environment Institute Helsinki Finland

5. Institute of Biotechnology, HILIFE ‐ Helsinki Institute for Life Science University of Helsinki Helsinki Finland

6. Ecology and Genetics Research Unit University of Oulu Oulu Finland

7. Tvärminne Zoological Station University of Helsinki Hanko Finland

8. Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics University of Amsterdam Amsterdam The Netherlands

Abstract

AbstractHybridisation and gene flow can have both deleterious and adaptive consequences for natural populations and species. To better understand the extent of hybridisation in nature and the balance between its beneficial and deleterious outcomes in a changing environment, information on naturally hybridising nonmodel organisms is needed. This requires the characterisation of the structure and extent of natural hybrid zones. Here, we study natural populations of five keystone mound‐building wood ant species in theFormica rufagroup across Finland. No genomic studies across the species group exist, and the extent of hybridisation and genomic differentiation in sympatry is unknown. Combining genome‐wide and morphological data, we demonstrate more extensive hybridisation than was previously detected between all five species in Finland. Specifically, we reveal a mosaic hybrid zone betweenFormica aquilonia,F. rufaandF. polyctena, comprising further generation hybrid populations. Despite this, we find thatF. rufa,F. aquilonia,F. lugubrisandF. pratensisform distinct gene pools in Finland. We also find that hybrids occupy warmer microhabitats than the nonadmixed populations of cold‐adaptedF. aquilonia, and suggest that warm winters and springs, in particular, may benefit hybrids overF. aquilonia, the most abundantF. rufagroup species in Finland. In summary, our results indicate that extensive hybridisation may create adaptive potential that could promote wood ant persistence in a changing climate. Additionally, they highlight the potentially significant ecological and evolutionary consequences of extensive mosaic hybrid zones, within which independent hybrid populations face an array of ecological and intrinsic selection pressures.

Funder

Academy of Finland

Societas pro Fauna et Flora Fennica

Publisher

Wiley

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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