A multiple peak adaptive landscape based on feeding strategies and roosting ecology shaped the evolution of cranial covariance structure and morphological differentiation in phyllostomid bats

Abstract

We explored the evolution of morphological integration in the most noteworthy example of adaptive radiation in mammals, the New World leaf‐nosed bats, using a massive dataset and by combining phylogenetic comparative methods and quantitative genetic approaches. We demonstrated that the phenotypic covariance structure remained conserved on a broader phylogenetic scale but also showed a substantial divergence between interclade comparisons. Most of the phylogenetic structure in the integration space can be explained by splits at the beginning of the diversification of major clades. Our results provide evidence for a multiple peak adaptive landscape in the evolution of cranial covariance structure and morphological differentiation, based upon diet and roosting ecology. In this scenario, the successful radiation of phyllostomid bats was triggered by the diversification of dietary and roosting strategies, and the invasion of these new adaptive zones lead to changes in phenotypic covariance structure and average morphology. Our results suggest that intense natural selection preceded the invasion of these new adaptive zones and played a fundamental role in shaping cranial covariance structure and morphological differentiation in this hyperdiverse clade of mammals. Finally, our study demonstrates the power of combining comparative methods and quantitative genetic approaches when investigating the evolution of complex morphologies.

Morphological Diversification under High Integration in a Hyper Diverse Mammal Clade

“…While this quantitative genetic approach is very different from the morphometric analyses typically used to investigate integration, it recovered the same signal of strong selection for divergent morphologies associated with dietary specialization found in previous studies (e.g., Freeman 1981;Dumont et al 2011Dumont et al , 2014Rossoni et al 2017). Rossoni et al (2019) provided an informative assessment of integration and morphological disparity within and among phyllostomids, but the study did not address whether and how phyllostomids differ from their close relatives. Here we extend the analysis of integration and disparity in the shape of the cranium to all families within the Superfamily Noctilionoidea: Noctilionidae, Mormoopidae, Mystacinidae, Furipteridae, and Thyropteridae.…”

“…With the exception of Old World fruit bats (Family Pteropodidae), all other bats are primarily insectivorous. Recently, Rossoni et al (2019) used a quantitative genetic approach to assess the evolution of morphological integration within the crania of phyllostomids. They found overarching commonalities in patterns of integration but striking differences among species with very different morphologies.…”

Dietary and body mass reconstruction of the Miocene neotropical batNotonycteris magdalenensis(Phyllostomidae) from La Venta, Colombia

“…Phyllostomidae is recognised as the greatest adaptive radiation of any mammalian family (Fleming et al 2020, Monteiro and Nogueira 2011, Rossoni et al 2017. Adoption of novel dietary niches and morphological innovation have been linked to the diversification of this family (Dumont et al 2012, Freeman 2000, Hedrick et al 2019, Rossoni et al 2019).…”

“…Loss or reduction of incisors and cheek teeth have been identified as convergent adaptations to liquid diets in Chiroptera (e.g., Freeman 1988, 1998, Berkovitz and Shellis 2018, Bolzan et al 2015). Nevertheless, sanguivorous and nectarivorous bats also show divergent specialised cranial morphologies adapted to each diet, with these dietary innovations following different evolutionary trajectories (Rossoni et al 2017, Rossoni et al 2019. Sanguivorous bats have a short rostrum, enlarged and procumbent upper incisors adapted for slicing, and reduced cheek teeth and lower incisors (Berkovitz and Shellis 2018).…”

“…Reconstructions of dietary evolution in Phyllostomidae suggest that carnivory and nectarivory evolved independently multiple times in different lineages, diverging from an insectivorous common ancestor (Datzmann et al 2010, Davies et al 2020, Rojas et al 2012, Santana and Cheung 2016. Morphological variability associated with diet-based functional demands is thought to have facilitated the ecological radiation and taxonomic diversification in Phyllostomidae (Arbour et al 2019, Hedrick et al 2019, Morales et al 2019, Rossoni et al 2019, Shi and Rabosky 2015Giannini et al 2020). Traditionally, most studies on dietary ecomorphology in bats have focused on skull morphology to study the form-function link, providing crucial information to understand the range of morphological specialisations (Aguirre et al 2002, Arbour et al 2019, Monteiro and Nogueira 2011, Rossoni et al 2019, Santana and Cheung 2016, Santana and Portugal 2016.…”