Evolutionary history and past climate change shape the distribution of genetic diversity in terrestrial mammals

Spyros Theodoridis,Stuart C Brown,David Nogues-Bravo,Damien A Fordham,Sen Li,Carsten Rahbek

doi:10.1038/s41467-020-16449-5

Spyros Theodoridis, Stuart C Brown + Show 4 more

Open Access

https://doi.org/10.1038/s41467-020-16449-5

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Abstract

Knowledge of global patterns of biodiversity, ranging from intraspecific genetic diversity (GD) to taxonomic and phylogenetic diversity, is essential for identifying and conserving the processes that shape the distribution of life. Yet, global patterns of GD and its drivers remain elusive. Here we assess existing biodiversity theories to explain and predict the global distribution of GD in terrestrial mammal assemblages. We find a strong positive covariation between GD and interspecific diversity, with evolutionary time, reflected in phylogenetic diversity, being the best predictor of GD. Moreover, we reveal the negative effect of past rapid climate change and the positive effect of inter-annual precipitation variability in shaping GD. Our models, explaining almost half of the variation in GD globally, uncover the importance of deep evolutionary history and past climate stability in accumulating and maintaining intraspecific diversity, and constitute a crucial step towards reducing the Wallacean shortfall for an important dimension of biodiversity.

Highlights

Knowledge of global patterns of biodiversity, ranging from intraspecific genetic diversity (GD) to taxonomic and phylogenetic diversity, is essential for identifying and conserving the processes that shape the distribution of life
Given that genetic variation is the raw material of species adaptive potential[19], and ecosystem resilience[2], there is a pressing need to establish whether a general relationship between GD and interspecific diversity exists, and predict its global distribution, in regions of the world that lack sufficient information
Our results show that the distribution of GD in terrestrial mammals positively covaries with other dimensions of biodiversity at the interspecific level (Figs. 1 and 2)

Summary

Introduction

Knowledge of global patterns of biodiversity, ranging from intraspecific genetic diversity (GD) to taxonomic and phylogenetic diversity, is essential for identifying and conserving the processes that shape the distribution of life. Increased data availability in past decades on species distributions and their evolutionary relationships, for mammals, has permitted global-scale evaluations of the distribution of two primary dimensions of biodiversity, namely species richness (SR) and PD3, allowing for their joint consideration as conservation targets[4,5] These advances have enabled in-depth assessments of how large-scale eco-evolutionary processes (speciation, extinction, and dispersal) shape latitudinal diversity gradients[6,7,8] and the mismatches between the spatiotemporal patterns of SR and PD9,10. A recent global assessment of the covariation between GD and species diversity in fish has shown a weak, yet significant, relationship[14], while regional studies have provided contrasting results, from no covariation in plants[15] and freshwater fish[16] to considerable overlap in coral reef fish[17] and amphibian and reptile assemblages[18] This has, precluded any generalization regarding the link between intra- and interspecific diversity at global scale and across phylogenetic clades. Overcoming the Wallacean shortfall for GD provides unique opportunities both in revealing the mechanisms that shape biodiversity in space and time, and in enhancing our predictions of how GD might change under ongoing and future environmental change[20]

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