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Abstract Geographic isolation is the primary driver of speciation in many vertebrate lineages. This trend is exemplified by North American darters, a clade of freshwater fishes where nearly all sister species pairs are allopatric and separated by millions of years of divergence. One of the only exceptions is the Lake Waccamaw endemic Etheostoma perlongum and its riverine sister species Etheostoma maculaticeps, which have no physical barriers to gene flow. Here we show that lacustrine speciation of E. perlongum is characterized by morphological and ecological divergence likely facilitated by a large chromosomal inversion. While E. perlongum is phylogenetically nested within the geographically widespread E. maculaticeps, there is a sharp genetic and morphological break coinciding with the lake–river boundary in the Waccamaw River system. Despite recent divergence, an active hybrid zone, and ongoing gene flow, analyses using a de novo reference genome reveal a 9 Mb chromosomal inversion with elevated divergence between E. perlongum and E. maculaticeps. This region exhibits striking synteny with known inversion supergenes in two distantly related fish lineages, suggesting deep evolutionary convergence of genomic architecture. Our results illustrate that rapid, ecological speciation with gene flow is possible even in lineages where geographic isolation is the dominant mechanism of speciation.
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Does Karyotype Structure Co‐Occurrence Patterns in a Chromosomally Diverse and Species‐Rich Clade of Lizards (Genus Sceloporus )?
ABSTRACT AimWe investigated the biogeographic consequences of chromosomal speciation, or structural changes in chromosome arrangement that lead to reproductive isolation, an intriguing speciation mechanism with implications for the phylogenetic and geographic distribution of species and chromosomal diversity. Location. North and Central America. Taxa. A species‐rich and chromosomally diverse clade of lizards in the genusSceloporuswhich are known to have coincident bursts of speciation and karyotype diversity, and coincident patterns of chromosomal change and branching order. Some workers have suggested that the tendency of communities ofSceloporuslizards to include species with different karyotypes is a signal of widespread chromosomal speciation, but given the high karyotypic diversity present inSceloporus, this may be due to chance rather than the effects of karyotypic speciation. MethodsWe gathered karyotypic, morphological, and biogeographic data on this chromosomally‐diverse clade in order to assess whether sympatry patterns ofSceloporusspecies are structured by karyotype. If karyotypic rearrangements contribute to the creation or maintenance of new species inSceloporus, then sympatric sister taxa should be more karyotypically diverged than allopatric sister taxa, and allopatric taxa should accumulate differences more gradually. We investigate whether species pairs with similar karyotypes are less likely to overlap geographically than expected by chance, and test whether karyotypic and geographic overlap between species pairs is related to divergence time. We pay special attention to cases of overlap between sister species. We also investigate whetherSceloporuscommunities are karyotypically overdispersed by comparing observed geographic distributions of karyotypic and phylogenetic diversity against phylogenetically‐informed modeled distributions. ResultsWe find little evidence for geographic signatures of chromosomal speciation and suggest that, while chromosomal speciation may have contributed historically to the spatial distributions ofSceloporusspecies, any geographic signature of this mode of speciation has been lost at long (> 10 Ma) temporal and broad (continental) spatial scales. Main ConclusionsThe spatial signature of chromosomal speciation is temporally restricted and the influences of other factors may have greater effects on species distributions over long time scales in this group.
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- Award ID(s):
- 2507670
- PAR ID:
- 10679590
- Publisher / Repository:
- Wiley, Journal of Biogeography
- Date Published:
- Journal Name:
- Journal of Biogeography
- Volume:
- 52
- Issue:
- 12
- ISSN:
- 0305-0270
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/jbi.70077
