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Abstract Determining the genetic architecture of traits involved in adaptation and speciation is one of the key components of understanding the evolutionary mechanisms behind biological diversification. Hybrid zones provide a unique opportunity to use genetic admixture to identify traits and loci contributing to partial reproductive barriers between taxa. Many studies have focused on the temporal dynamics of hybrid zones, but geographical variation in hybrid zones that span distinct ecological contexts has received less attention. We address this knowledge gap by analyzing hybridization and introgression between black-capped and Carolina chickadees in two geographically remote transects across their extensive hybrid zone, one located in eastern and one in central North America. Previous studies demonstrated that this hybrid zone is moving northward as a result of climate change but is staying consistently narrow due to selection against hybrids. In addition, the hybrid zone is moving ~5× slower in central North America compared to more eastern regions, reflecting continent-wide variation in the rate of climate change. We use whole genome sequencing of 259 individuals to assess whether variation in the rate of hybrid zone movement is reflected in patterns of hybridization and introgression, and which genes and genomic regions show consistently restricted introgression in distinct ecological contexts. Our results highlight substantial similarities between geographically remote transects and reveal large Z-linked chromosomal rearrangements that generate measurable differences in the degree of gene flow between transects. We further use simulations and analyses of climatic data to examine potential factors contributing to continental-scale nuances in selection pressures. We discuss our findings in the context of speciation mechanisms and the importance of sex chromosome inversions in chickadees and other species.
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This content will become publicly available on October 1, 2025
Understanding species limits through the formation of phylogeographic lineages
Abstract The outcomes of speciation across organismal dimensions (e.g., ecological, genetic, phenotypic) are often assessed using phylogeographic methods. At one extreme, reproductively isolated lineages represent easily delimitable species differing in many or all dimensions, and at the other, geographically distinct genetic segments introgress across broad environmental gradients with limited phenotypic disparity. In the ambiguous gray zone of speciation, where lineages are genetically delimitable but still interacting ecologically, it is expected that these lineages represent species in the context of ontology and the evolutionary species concept when they are maintained over time with geographically well‐defined hybrid zones, particularly at the intersection of distinct environments. As a result, genetic structure is correlated with environmental differences and not space alone, and a subset of genes fail to introgress across these zones as underlying genomic differences accumulate. We present a set of tests that synthesize species delimitation with the speciation process. We can thereby assess historical demographics and diversification processes while understanding how lineages are maintained through space and time by exploring spatial and genome clines, genotype‐environment interactions, and genome scans for selected loci. Employing these tests in eight lineage‐pairs of snakes in North America, we show that six pairs represent 12 “good” species and that two pairs represent local adaptation and regional population structure. The distinct species pairs all have the signature of divergence before or near the mid‐Pleistocene, often with low migration, stable hybrid zones of varying size, and a subset of loci showing selection on alleles at the hybrid zone corresponding to transitions between distinct ecoregions. Locally adapted populations are younger, exhibit higher migration, and less ecological differentiation. Our results demonstrate that interacting lineages can be delimited using phylogeographic and population genetic methods that properly integrate spatial, temporal, and environmental data.
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- Award ID(s):
- 1831241
- PAR ID:
- 10560509
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 14
- Issue:
- 10
- ISSN:
- 2045-7758
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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