Intense natural selection preceded the invasion of new adaptive zones during the radiation of New World leaf-nosed bats

Daniela M Rossoni,Gabriel Marroig,Ana Paula A Assis,Norberto P Giannini

doi:10.1038/s41598-017-08989-6

Abstract

The family Phyllostomidae, which evolved in the New World during the last 30 million years, represents one of the largest and most morphologically diverse mammal families. Due to its uniquely diverse functional morphology, the phyllostomid skull is presumed to have evolved under strong directional selection; however, quantitative estimation of the strength of selection in this extraordinary lineage has not been reported. Here, we used comparative quantitative genetics approaches to elucidate the processes that drove cranial evolution in phyllostomids. We also quantified the strength of selection and explored its association with dietary transitions and specialization along the phyllostomid phylogeny. Our results suggest that natural selection was the evolutionary process responsible for cranial diversification in phyllostomid bats. Remarkably, the strongest selection in the phyllostomid phylogeny was associated with dietary specialization and the origination of novel feeding habits, suggesting that the adaptive diversification of phyllostomid bats was triggered by ecological opportunities. These findings are consistent with Simpson’s quantum evolutionary model of transitions between adaptive zones. The multivariate analyses used in this study provides a powerful tool for understanding the role of evolutionary processes in shaping phenotypic diversity in any group on both micro- and macroevolutionary scales.

Highlights

The New World leaf-nosed bats, family Phyllostomidae, are arguably the most ecologically diverse group of mammals6
In order to assess the evolutionary processes responsible for the diversification of cranial morphology in phyllostomid bats, we used two drift tests, a regression test and a correlation test. Both tests are grounded in quantitative genetics theory and are based on the expectation that under neutral evolution, the direction and magnitude of multivariate variance-covariance evolution should be proportional to the ancestral covariance patterns28–30
These plots show that significant deviations in regression slopes from expectations based on drift were largely due to variation in the first principal component (PC1)

Summary

Introduction

The New World leaf-nosed bats, family Phyllostomidae, are arguably the most ecologically diverse group of mammals. Phyllostomids have a distribution ranging from southern Arizona and the West Indies to northern Argentina, and have been highly successful in exploiting a diverse array of resources6 These bats have evolved over the last 30 million years, and their dietary breadth and feeding habits are exceptionally diverse compared with other mammals; the family includes species highly specialized for feeding on insects, vertebrates, fruit, pollen, nectar, young leaves, and even blood. These bats have evolved over the last 30 million years, and their dietary breadth and feeding habits are exceptionally diverse compared with other mammals; the family includes species highly specialized for feeding on insects, vertebrates, fruit, pollen, nectar, young leaves, and even blood6 This ecological diversification is reflected in phyllostomid morphology, which shows wide variation in body size and shape, in the skull. We expected the evolution of dietary specializations and novel feeding habits along the phyllostomid phylogeny to be associated with stronger selection magnitudes

Methods

Results

Discussion

Conclusion