Abstract Speciation rates vary substantially across the tree of life. These rates should be linked to the rate at which population structure forms if a continuum between micro and macroevolutionary patterns exists. Previous studies examining the link between speciation rates and the degree of population formation in clades have been shown to be either correlated or uncorrelated depending on the group, but no study has yet examined the relationship between speciation rates and population structure in a young group that is constrained spatially to a single‐island system. We examine this correlation in 109 gemsnakes (Pseudoxyrhophiidae) endemic to Madagascar and originating in the early Miocene, which helps control for extinction variation across time and space. We find no relationship between rates of speciation and the formation rates of population structure over space in 33 species of gemsnakes. Rates of speciation show low variation, yet population structure varies widely across species, indicating that speciation rates and population structure are disconnected. We suspect this is largely due to the persistence of some lineages not susceptible to extinction. Importantly, we discuss how delimiting populations versus species may contribute to problems understanding the continuum between shallow and deep evolutionary processes. 
                        more » 
                        « less   
                    
                            
                            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   
        
    
                            - Award ID(s):
- 1754398
- PAR ID:
- 10326538
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 119
- Issue:
- 4
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
- 
            
- 
            PremiseDivergence 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. MethodsUsing 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. ResultsWe 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. ConclusionsPatterns 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.more » « less
- 
            Mating cues evolve rapidly and can contribute to species formation and maintenance. However, little is known about how sexual signals diverge and how this variation integrates with other barrier loci to shape the genomic landscape of reproductive isolation. Here, we elucidate the genetic basis of ultraviolet (UV) iridescence, a courtship signal that differentiates the males of Colias eurytheme butterflies from a sister species, allowing females to avoid costly heterospecific matings. Anthropogenic range expansion of the two incipient species established a large zone of secondary contact across the eastern United States with strong signatures of genomic admixtures spanning all autosomes. In contrast, Z chromosomes are highly differentiated between the two species, supporting a disproportionate role of sex chromosomes in speciation known as the large-X (or large-Z) effect. Within this chromosome-wide reproductive barrier, linkage mapping indicates that cis- regulatory variation of bric a brac ( bab ) underlies the male UV-iridescence polymorphism between the two species. Bab is expressed in all non-UV scales, and butterflies of either species or sex acquire widespread ectopic iridescence following its CRISPR knockout, demonstrating that Bab functions as a suppressor of UV-scale differentiation that potentiates mating cue divergence. These results highlight how a genetic switch can regulate a premating signal and integrate with other reproductive barriers during intermediate phases of speciation.more » « less
- 
            • 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.more » « less
- 
            Olfaction is an important sense that has contributed to reproductive isolation and speciation in many taxa. However, in birds, olfaction and its potential role in communication has historically been neglected. Thus, what role olfaction plays in avian speciation is mostly unknown. Here, we aim to guide future research by highlighting the likely potential for olfaction to contribute to reproductive isolation and speciation in birds. First, we detail the best-understood example found thus far that is consistent with reproductive isolation by olfaction in birds: black-capped and Carolina chickadees. These species show interspecific differences in preen oil chemistry and conspecific odour preferences within their natural hybrid zone. We then suggest a number of promising avenues for future research and the kinds of systems, approaches and evidence that would help to advance this severely understudied area. In sum, the growing body of research into the chemical ecology of birds suggests an important role of olfaction in many areas of avian life. Future research will be necessary to determine to what extent olfaction contributes to the formation and maintenance of species boundaries in birds.more » « less
 An official website of the United States government
An official website of the United States government 
				
			 
					 
					
 
                                    