Title: No link between population isolation and speciation rate in squamate reptiles
Rates of species formation vary widely across the tree of life and contribute to massive disparities in species richness among clades. This variation can emerge from differences in metapopulation-level processes that affect the rates at which lineages diverge, persist, and evolve reproductive barriers and ecological differentiation. For example, populations that evolve reproductive barriers quickly should form new species at faster rates than populations that acquire reproductive barriers more slowly. This expectation implicitly links microevolutionary processes (the evolution of populations) and macroevolutionary patterns (the profound disparity in speciation rate across taxa). Here, leveraging extensive field sampling from the Neotropical Cerrado biome in a biogeographically controlled natural experiment, we test the role of an important microevolutionary process—the propensity for population isolation—as a control on speciation rate in lizards and snakes. By quantifying population genomic structure across a set of codistributed taxa with extensive and phylogenetically independent variation in speciation rate, we show that broad-scale patterns of species formation are decoupled from demographic and genetic processes that promote the formation of population isolates. Population isolation is likely a critical stage of speciation for many taxa, but our results suggest that interspecific variability in the propensity for isolation has little influence on speciation rates. These results suggest that other stages of speciation—including the rate at which reproductive barriers evolve and the extent to which newly formed populations persist—are likely to play a larger role than population isolation in controlling speciation rate variation in squamates. more »« less
Wenzell, Katherine E.; McDonnell, Angela J.; Wickett, Norman J.; Fant, Jeremie B.; Skogen, Krissa A.(
, American Journal of Botany)
Premise
Divergence depends on the strength of selection and frequency of gene flow between taxa, while reproductive isolation relies on mating barriers and geographic distance. Less is known about how these processes interact at early stages of speciation. Here, we compared population‐level differentiation in floral phenotype and genetic sequence variation among recently divergedCastillejato explore patterns of diversification under different scenarios of reproductive isolation.
Methods
Using target enrichment enabled by the Angiosperms353 probe set, we assessed genetic distance among 50 populations of fourCastillejaspecies. We investigated whether patterns of genetic divergence are explained by floral trait variation or geographic distance in two focal groups: the widespreadC. sessilifloraand the more restrictedC. purpureaspecies complex.
Results
We document thatC. sessilifloraand theC. purpureacomplex are characterized by high diversity in floral color across varying geographic scales. Despite phenotypic divergence, groups were not well supported in phylogenetic analyses, and little genetic differentiation was found across targeted Angiosperms353 loci. Nonetheless, a principal coordinate analysis of single nucleotide polymorphisms revealed differentiation withinC. sessilifloraacross floral morphs and geography and less differentiation among species of theC. purpureacomplex.
Conclusions
Patterns of genetic distance inC. sessiliflorasuggest species cohesion maintained over long distances despite variation in floral traits. In theC. purpureacomplex, divergence in floral color across narrow geographic clines may be driven by recent selection on floral color. These contrasting patterns of floral and genetic differentiation reveal that divergence can arise via multiple eco‐evolutionary paths.
Shahid, Bushra M.; Burgin, Grace A.; Hopkins, Robin(
, International Journal of Plant Sciences)
• Reinforcement is the process through which prezygotic reproductive barriers evolve in sympatry due to selection against hybridization between co-occurring, closely related species. The role of self-fertilization in reinforcement and reproductive isolation is uncertain in part because its efficiency as a barrier against heterospecific mating can depend on the timing of autonomous selfing.
• To investigate whether increased autonomous selfing has evolved as a mechanism for reinforcement, we compared Phlox cuspidata populations across their native Texas range using both estimates of genetic diversity and experimental manipulation with morphological measurements. Specifically, we investigated patterns of variation in floral traits and timing of selfing between individuals from allopatric populations of P. cuspidata and from populations sympatric with the closely related species, P. drummondii.
• We infer intermediate rates of selfing across field-collected individuals with no significant difference between allopatric and sympatric populations. Among greenhouse grown plants, we find no differences in timing of selfing or other floral traits including anther dehiscence timing, anther-stigma distances, autonomous selfing rate and self-seed count between allopatric and sympatric populations. However, our statistical analyses indicate that P. cuspidata individuals sympatric with P drummondii seem to have generally larger flowers compared to allopatric individuals.
• Despite strong evidence of costly hybridization with P. drummondii, we find no evidence of trait divergence due to reinforcement in P. cuspidata. Although we document nearly complete autonomous self-seed set in the greenhouse, estimates of selfing rates from genetic data imply realized selfing is much lower in nature suggesting an opportunity for reinforcing selection to act on this trait.
Scherrer, Raphaël; Donihue, Colin M.; Reynolds, Robert Graham; Losos, Jonathan B.; Geneva, Anthony J.(
, Journal of Evolutionary Biology)
Abstract
Animal signals evolve in an ecological context. Locally adapting animal sexual signals can be especially important for initiating or reinforcing reproductive isolation during the early stages of speciation. Previous studies have demonstrated that dewlap colour inAnolislizards can be highly variable between populations in relation to both biotic and abiotic adaptive drivers at relatively large geographical scales. Here, we investigated differentiation of dewlap colouration among habitat types at a small spatial scale, within multiple islands of the West Indies, to test the hypothesis that similar local adaptive processes occur over smaller spatial scales. We explored variation in dewlap colouration in the most widespread species of anole,Anolis sagrei, across three characteristic habitats spanning the Bahamas and the Cayman Islands, namely beach scrub, primary coppice forest and mangrove forest. Using reflectance spectrometry paired with supervised machine learning, we found significant differences in spectral properties of the dewlap between habitats within small islands, sometimes over very short distances. Passive divergence in dewlap phenotype associated with isolation‐by‐distance did not seem to explain our results. On the other hand, these habitat‐specific dewlap differences varied in magnitude and direction across islands, and thus, our primary test for adaptation—parallel responses across islands—was not supported. We suggest that neutral processes or selection could be involved in several ways, including sexual selection. Our results shed new light on the scale at which signal colour polymorphism can be maintained in the presence of gene flow, and the relative role of local adaptation and other processes in driving these patterns of dewlap colour variation across islands.
Kenney, Amanda M.; Sweigart, Andrea L.(
, Molecular Ecology)
Abstract
Incompletely isolated species provide an opportunity to investigate the genetic mechanisms and evolutionary forces that maintain distinct species in the face of ongoing gene flow. Here, we use field surveys and reduced representation sequencing to characterize the patterns of reproductive isolation, admixture and genomic divergence between populations of the outcrossing wildflowerMimulus guttatusand selfingM. nasutus. Focusing on a single site where these two species have come into secondary contact, we find that phenological isolation is strong, although incomplete, and is likely driven by divergence in response to photoperiod. In contrast to previous field studies, which have suggested that F1‐hybrid formation might be rare, we discover patterns of genomic variation consistent with ongoing introgression. Strikingly, admixed individuals vary continuously from highly admixed to nearly pureM. guttatus, demonstrating ongoing hybridization and asymmetric introgression fromM. nasutusintoM. guttatus. Patterns of admixture and divergence across the genome show that levels of introgression are more variable than expected by chance. Some genomic regions show a reduced introgression, including one region that overlaps a critical photoperiodQTL, whereas other regions show elevated levels of interspecific gene flow. In addition, we observe a genome‐wide negative relationship between absolute divergence and the local recombination rate, potentially indicating natural selection againstM. nasutusancestry inM. guttatusgenetic backgrounds. Together, our results suggest thatMimulusspeciation is both ongoing and dynamic and that a combination of divergence in phenology and mating system, as well as selection against interspecific alleles, likely maintains these sympatric species.
Pyron, R. Alexander; Kakkera, Anvith; Beamer, David A.; O'Connell, Kyle A.(
, Molecular Ecology)
Abstract
Numerous mechanisms can drive speciation, including isolation by adaptation, distance, and environment. These forces can promote genetic and phenotypic differentiation of local populations, the formation of phylogeographic lineages, and ultimately, completed speciation. However, conceptually similar mechanisms may also result in stabilizing rather than diversifying selection, leading to lineage integration and the long‐term persistence of population structure within genetically cohesive species. Processes that drive the formation and maintenance of geographic genetic diversity while facilitating high rates of migration and limiting phenotypic differentiation may thereby result in population genetic structure that is not accompanied by reproductive isolation. We suggest that this framework can be applied more broadly to address the classic dilemma of “structure” versus “species” when evaluating phylogeographic diversity, unifying population genetics, species delimitation, and the underlying study of speciation. We demonstrate one such instance in the Seepage Salamander (Desmognathus aeneus) from the southeastern United States. Recent studies estimated up to 6.3% mitochondrial divergence and four phylogenomic lineages with broad admixture across geographic hybrid zones, which could potentially represent distinct species supported by our species‐delimitation analyses. However, while limited dispersal promotes substantial isolation by distance, microhabitat specificity appears to yield stabilizing selection on a single, uniform, ecologically mediated phenotype. As a result, climatic cycles promote recurrent contact between lineages and repeated instances of high migration through time. Subsequent hybridization is apparently not counteracted by adaptive differentiation limiting introgression, leaving a single unified species with deeply divergent phylogeographic lineages that nonetheless do not appear to represent incipient species.
Singhal, Sonal, Colli, Guarino R., Grundler, Maggie R., Costa, Gabriel C., Prates, Ivan, and Rabosky, Daniel L. No link between population isolation and speciation rate in squamate reptiles. Retrieved from https://par.nsf.gov/biblio/10326538. Proceedings of the National Academy of Sciences 119.4 Web. doi:10.1073/pnas.2113388119.
Singhal, Sonal, Colli, Guarino R., Grundler, Maggie R., Costa, Gabriel C., Prates, Ivan, & Rabosky, Daniel L. No link between population isolation and speciation rate in squamate reptiles. Proceedings of the National Academy of Sciences, 119 (4). Retrieved from https://par.nsf.gov/biblio/10326538. https://doi.org/10.1073/pnas.2113388119
Singhal, Sonal, Colli, Guarino R., Grundler, Maggie R., Costa, Gabriel C., Prates, Ivan, and Rabosky, Daniel L.
"No link between population isolation and speciation rate in squamate reptiles". Proceedings of the National Academy of Sciences 119 (4). Country unknown/Code not available. https://doi.org/10.1073/pnas.2113388119.https://par.nsf.gov/biblio/10326538.
@article{osti_10326538,
place = {Country unknown/Code not available},
title = {No link between population isolation and speciation rate in squamate reptiles},
url = {https://par.nsf.gov/biblio/10326538},
DOI = {10.1073/pnas.2113388119},
abstractNote = {Rates of species formation vary widely across the tree of life and contribute to massive disparities in species richness among clades. This variation can emerge from differences in metapopulation-level processes that affect the rates at which lineages diverge, persist, and evolve reproductive barriers and ecological differentiation. For example, populations that evolve reproductive barriers quickly should form new species at faster rates than populations that acquire reproductive barriers more slowly. This expectation implicitly links microevolutionary processes (the evolution of populations) and macroevolutionary patterns (the profound disparity in speciation rate across taxa). Here, leveraging extensive field sampling from the Neotropical Cerrado biome in a biogeographically controlled natural experiment, we test the role of an important microevolutionary process—the propensity for population isolation—as a control on speciation rate in lizards and snakes. By quantifying population genomic structure across a set of codistributed taxa with extensive and phylogenetically independent variation in speciation rate, we show that broad-scale patterns of species formation are decoupled from demographic and genetic processes that promote the formation of population isolates. Population isolation is likely a critical stage of speciation for many taxa, but our results suggest that interspecific variability in the propensity for isolation has little influence on speciation rates. These results suggest that other stages of speciation—including the rate at which reproductive barriers evolve and the extent to which newly formed populations persist—are likely to play a larger role than population isolation in controlling speciation rate variation in squamates.},
journal = {Proceedings of the National Academy of Sciences},
volume = {119},
number = {4},
author = {Singhal, Sonal and Colli, Guarino R. and Grundler, Maggie R. and Costa, Gabriel C. and Prates, Ivan and Rabosky, Daniel L.},
}
Warning: Leaving National Science Foundation Website
You are now leaving the National Science Foundation website to go to a non-government website.
Website:
NSF takes no responsibility for and exercises no control over the views expressed or the accuracy of
the information contained on this site. Also be aware that NSF's privacy policy does not apply to this site.