A multi‐layered approach to the diversification of squirrels

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The shape of the tree of life is the result of shifting diversification rates, and identifying the factors driving these shifts is one of the main aims in evolutionary biology. Various biotic and abiotic factors have been proposed to have an impact on mammal diversification, such as climatic and tectonic changes, the acquisition of new traits, and expansion into new ecosystems or landmasses. We used phylogenetic comparative methods to quantify the influence of potential drivers on diversification patterns in extant squirrels (Sciuridae, Rodentia). We conducted a multilayer approach, comparing diversification rates among squirrel lineages depending on their degree of biome specialisation, biogeographic realm occupancy, locomotion adaptations, and presence in mountainous regions. We generated the most complete phylogeny of squirrels to date, encompassing almost 80% of the extant species, and applied multiple and binary state‐dependent diversification models. All the traits examined showed an influence on diversification rates. The biome specialist lineages showed the highest speciation rates, suggesting a major role of bioclimatic specialisation on macroevolutionary patterns. A single major event, the Miocene–Pleistocene radiation of terrestrial‐adapted lineages in North America, left a signal that was recovered in two of our analyses. Both the Nearctic lineages and the terrestrial‐adapted lineages showed high speciation rates, highlighting the fact that that major evolutionary episodes may produce confounding effects in state‐dependent diversification models. Ancestral reconstructions showed that cold and warm intervals in Earth’s history had different effects on squirrels’ diversification, depending on their climatic affinities. Tropical and arboreal squirrels evolved predominantly in the warm intervals, while terrestrial and cold‐adapted squirrels radiated in the cold intervals. Our findings suggest that, while global climatic shifts are key for the speciation processes in mammalian lineages, lineage‐specific ecological adaptations are critical modulators of the responses of lineages to such environmental shifts, in an interplay that ultimately affects their diversification patterns.
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