Does Population Structure Predict the Rate of Speciation? A Comparative Test across Australia’s Most Diverse Vertebrate Radiation

Singhal, Sonal; Huang, Huateng; Grundler, Maggie R.; Marchán-Rivadeneira, María R.; Holmes, Iris; Title, Pascal O.; Donnellan, Stephen C.; Rabosky, Daniel L.

doi:10.1086/699515

Cited by 52 publications

(66 citation statements)

References 108 publications

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“…Direct tests on the influence of population differentiation on speciation rates are thus necessary in order to establish whether population differentiation is a rate‐limiting step of the speciation process (Harvey et al., 2019). Such tests are scarce and have only focused on vertebrates, finding a positive association in New World birds (Harvey et al., 2017), and no association in Australian lizards (Singhal et al., 2018). We encourage similar tests in seed plants at a global scale.…”

Section: Discussionmentioning

confidence: 99%

Global patterns of population genetic differentiation in seed plants

Gamba

Muchhala

2020

Molecular Ecology

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Evaluating the factors that drive patterns of population differentiation in plants is critical for understanding several biological processes such as local adaptation and incipient speciation. Previous studies have given conflicting results regarding the significance of pollination mode, seed dispersal mode, mating system, growth form and latitudinal region in shaping patterns of genetic structure, as estimated by FST values, and no study to date has tested their relative importance together across a broad scale. Here, we assembled a 337‐species data set for seed plants from publications with data on FST from nuclear markers and species traits, including variables pertaining to the sampling scheme of each study. We used species traits, while accounting for sampling variables, to perform phylogenetic multiple regressions. Results demonstrated that FST values were higher for tropical, mixed‐mating, non‐woody species pollinated by small insects, indicating greater population differentiation, and lower for temperate, outcrossing trees pollinated by wind. Among the factors we tested, latitudinal region explained the largest portion of variance, followed by pollination mode, mating system and growth form, while seed dispersal mode did not significantly relate to FST. Our analyses provide the most robust and comprehensive evaluation to date of the main ecological factors predicted to drive population differentiation in seed plants, with important implications for understanding the basis of their genetic divergence. Our study supports previous findings showing greater population differentiation in tropical regions and is the first that we are aware of to robustly demonstrate greater population differentiation in species pollinated by small insects.

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Section: Discussionmentioning

confidence: 99%

Global patterns of population genetic differentiation in seed plants

Gamba

Muchhala

2020

Molecular Ecology

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“…Moreover, theory and simulation studies indicate that F ST broadly reflects the rate of gene flow even when strict assumptions of the island model are violated (Slatkin and Barton 1989; Slatkin 1993), and F ST correlates well with gene flow over longer evolutionary timescales (Bohonak 1999; Singhal et al. 2018). Results for all measures of genetic similarity will be presented, but our discussion in the main text will focus on the effective number of migrants because F ST ‐related quantities are by far the most common metric of divergence used in studies of population structure and landscape genetics (Jenkins et al.…”

Section: Methodsmentioning

confidence: 99%

Relative importance of isolation‐by‐environment and other determinants of gene flow in an alpine amphibian

Buskirk

Rensburg

2020

Evolution

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A pattern of population structure called isolation-by-environment (IBE) evolves when gene flow connecting populations in different habitats is lower than expected. Although IBE is widespread, there is limited information on its magnitude compared with other factors influencing gene flow. We estimated the relative importance of IBE in the frog Rana temporaria in the Swiss Alps, a geographic context in which IBE should be relatively pronounced. The environmental factor potentially causing IBE was the length of the growing season, which is highly correlated with elevation. A sample of 992 individuals from 82 breeding sites were genotyped at 1827 single-nucleotide polymorphism markers; gene flow was estimated in four ways related to F ST , genetic distance, allele sharing, and distance on a population graph. Gravity modeling and random forest regression evaluated the importance of six at-site covariates, 10 between-site covariates, and geographic distance. There was broad agreement among analysis methods and measures of gene flow: isolation-by-distance (IBD) and habitat quality between sites were of highest importance, the elevation and ruggedness of the dispersal path were about half as important, and IBE was about 10-20% as important as IBD. These results combine with other evidence to suggest that population divergence across elevational gradients is underway in amphibians. K E Y W O R D S : Altitude, connectivity, ddRAD, isolation-by-adaptation, topography. Clearly, the alternative habitats must impose divergent selection on traits that influence gene flow (Widmer et al. 2009; Wang and Bradburd 2014; Butlin and Smadja 2018). Selection imposed by phenological differences between habitats has attracted particular 9 6 2

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“…Dynamics between and within populations are the stepping stone linking genetic diversity with species richness (Fine, 2015;Marchesini et al, 2018;Marske et al, 2013;Paz-Vinas et al, 2018;Singhal et al, 2018). Increasing genetic differentiation leads to population divergence and eventually speciation due to isolation and/or selection (Schluter, 2016;Schluter & Pennell, 2017;Taylor, 1999;Wiens, 2004).…”

Section: Introductionmentioning

confidence: 99%

Latitudinal biodiversity gradients at three levels: Linking species richness, population richness and genetic diversity

Lawrence

Fraser

2020

Global Ecol Biogeogr

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Motivation Theory describing biodiversity gradients has focused on species richness with less conceptual synthesis outlining expectations for intraspecific diversity gradients, that is, broad‐scale population richness and genetic diversity. Consequently, there is a need for a diversity–gradient synthesis that complements species richness with population richness and genetic diversity. Review methods Species and population richness are the number of different species or populations in an area, respectively. Population richness can be totalled across species, within a species or averaged across species. Genetic diversity within populations can be summed or averaged across all species in an area or be averaged across an individual species. Using these definitions, we apply historical, ecological and evolutionary frameworks of species richness gradients to formulate predictions for intraspecific diversity gradients. Review conclusions All frameworks suggest higher average population richness at high latitudes, but similar total population richness across latitudes. Predictions for genetic diversity patterns across species are not consistent across frameworks and latitudes. New analysis methods Species range size tends to increase with latitude, so we used empirical data from c. 900 vertebrate species to test hypotheses relating species range size and richness to population richness and genetic diversity. New analysis conclusions Species range size was positively associated with its population richness but not with species‐specific genetic diversity. Furthermore, a positive linear relationship was supported between species richness and total population richness, but only weakly for average population richness. Overall conclusion Through the lens of species richness theories, our synthesis identifies an uncoupling between species richness, population richness and genetic diversity in many instances due to historical and contemporary factors. Range size and taxonomic differences appear to play a large role in moderating intraspecific diversity gradients. We encourage further analyses to jointly assess diversity–gradient theory at species, population and genetic levels towards better understanding Earth’s biodiversity distribution and refining biodiversity conservation.

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Does Population Structure Predict the Rate of Speciation? A Comparative Test across Australia’s Most Diverse Vertebrate Radiation

Cited by 52 publications

References 108 publications

Global patterns of population genetic differentiation in seed plants

Global patterns of population genetic differentiation in seed plants

Relative importance of isolation‐by‐environment and other determinants of gene flow in an alpine amphibian

Latitudinal biodiversity gradients at three levels: Linking species richness, population richness and genetic diversity

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