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Abstract Understanding the genetics of adaptation and speciation is critical for a complete picture of how biodiversity is generated and maintained. Heterogeneous genomic differentiation between diverging taxa is commonly documented, with genomic regions of high differentiation interpreted as resulting from differential gene flow, linked selection and reduced recombination rates. Disentangling the roles of each of these non‐exclusive processes in shaping genome‐wide patterns of divergence is challenging but will enhance our knowledge of the repeatability of genomic landscapes across taxa. Here, we combine whole‐genome resequencing and genome feature data to investigate the processes shaping the genomic landscape of differentiation for a sister‐species pair of haplodiploid pine sawflies,Neodiprion leconteiandNeodiprion pinetum. We find genome‐wide correlations between genome features and summary statistics are consistent with pervasive linked selection, with patterns of diversity and divergence more consistently predicted by exon density and recombination rate than the neutral mutation rate (approximated by dS). We also find that both global and local patterns ofFST,dXYandπprovide strong support for recurrent selection as the primary selective process shaping variation across pine sawfly genomes, with some contribution from balancing selection and lineage‐specific linked selection. Because inheritance patterns for haplodiploid genomes are analogous to those of sex chromosomes, we hypothesize that haplodiploids may be especially prone to recurrent selection, even if gene flow occurred throughout divergence. Overall, our study helps fill an important taxonomic gap in the genomic landscape literature and contributes to our understanding of the processes that shape genome‐wide patterns of genetic variation.
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Recombination Rate and Recurrent Linked Selection Shape Correlated Genomic Landscapes Across a Continuum of Divergence in Swallows
ABSTRACT Disentangling the drivers of genomic divergence during speciation is essential to our broader understanding of the generation of biological diversity. Genetic changes accumulate at variable rates across the genome as populations diverge, leading to heterogenous landscapes of genetic differentiation. The ‘islands of differentiation’ that characterise these landscapes harbour genetic signatures of the evolutionary processes that led to their formation, providing insight into the roles of these processes in adaptation and speciation. Here, we study swallows in the genusHirundoto investigate genomic landscapes of differentiation between species spanning a continuum of evolutionary divergence. Genomic differentiation spans a wide range of values (FST= 0.01–0.8) between species, with substantial heterogeneity in genome‐wide patterns. Genomic landscapes are strongly correlated among species (ρ= 0.46–0.99), both at shallow and deep evolutionary timescales, with broad evidence for the role of linked selection together with recombination rate in shaping genomic differentiation. Further dissection of genomic islands reveals patterns consistent with a model of ‘recurrent selection’, wherein differentiation increases due to selection in the same genomic regions in ancestral and descendant populations. Finally, we use measures of the site frequency spectrum to differentiate between alternative forms of selection, providing evidence that genetic hitchhiking due to positive selection has contributed substantially to genomic divergence. Our results demonstrate the pervasive role of recurrent linked selection in shaping genomic divergence despite a history of gene flow and underscore the importance of non‐neutral evolutionary processes in predictive frameworks for genomic divergence in speciation genomics studies.
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- Award ID(s):
- 1856266
- PAR ID:
- 10647494
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 34
- Issue:
- 22
- ISSN:
- 0962-1083
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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