Peramorphosis, an evolutionary developmental mechanism in neotropical bat skull diversity

Abstract

Background The neotropical leaf‐nosed bats (Chiroptera, Phyllostomidae) are an ecologically diverse group of mammals with distinctive morphological adaptations associated with specialized modes of feeding. The dramatic skull shape changes between related species result from changes in the craniofacial development process, which brings into focus the nature of the underlying evolutionary developmental processes. Results In this study, we use three‐dimensional geometric morphometrics to describe, quantify, and compare morphological modifications unfolding during evolution and development of phyllostomid bats. We examine how changes in development of the cranium may contribute to the evolution of the bat craniofacial skeleton. Comparisons of ontogenetic trajectories to evolutionary trajectories reveal two separate evolutionary developmental growth processes contributing to modifications in skull morphogenesis: acceleration and hypermorphosis. Conclusion These findings are consistent with a role for peramorphosis, a form of heterochrony, in the evolution of bat dietary specialists.

Differential cellular proliferation underlies heterochronic generation of cranial diversity in phyllostomid bats

“…We hypothesized that if the alteration in developmental timing occurred at the cellular level, we would expect a localized temporal change in cell proliferation when compared to the ancestral mode of development. More specifically, compared to the ancestor, we anticipated a higher rate of proliferation in fruit bats and a more extended period of cell proliferation in nectar bats associated with acceleration and hypermorphosis, respectively, as we previously detected in these taxa morphologically [11].…”

“…The "Irish elk", an extinct deer species with enormous exaggerated antlers, is a textbook example of peramorphosis [26]. Our recent morphometric studies on adult, juvenile and embryonic skulls demonstrated that several skull shapes within phyllostomid cranial diversity evolved by peramorphosis [11]. Long-faced nectar-eating (subfamily Glossophaginae) and short-faced blood-eating (subfamily Desmondontinae) bats generate ecomorphspecific skulls by extending the ancestral ontogenetic program and appending new late developmental stages, thus demonstrating peramorphosis by hypermorphosis [3].…”

“…Here, we investigate cellular proliferation underlying distinct morphogenetic trajectories in facial development caused by peramorphosis in phyllostomid bats. Our previous geometric morphometric analysis of phyllostomid skull shape showed that the most significant axis of morphologic change was the length of the skull and snout [11], which was captured by principal component (PC) 1 (Fig. 2).…”

A Culture-Based ID of Micromycetes on the Wing Membranes of Greater Mouse-Eared Bats (Myotis myotis) from the “Nietoperek” Site (Poland)

“…Bats (Chiroptera), inhabiting all continents except Antarctica, with more than 1400 species described so far, are the second most numerous order among all mammals [1,2]. Most species are insectivorous and serve an important role in the reduction of insect abundance, including agricultural and forest pests, and species harmful for humans such as mosquitoes (Culicidae) and biting midges (Simuliidae and Ceratopogonidae) [3], although in the tropics many bats developed different feeding strategies and serve as plant pollinators and seed dispersers [4]. Almost half of bats are vulnerable (VU), considered endangered (EN), near threatened (NT) or critically endangered (CR) and are listed in the IUCN Red List of Endangered Species [5,6].…”

Evo‐devo explores the endless forms most beautiful, from extreme traits to subtle diversities

“…By analyzing bones on a detailed micro‐anatomical level and relating developmental changes to the external anatomy, limb function and changes in animal behavior as maturation commences, Montoya‐Sanhueza et al reveal how a combination of both genetic and behavioral factors related to digging likely impact the process of mole rat limb maturation. Similarly, Camacho et al use 3D geometric morphometrics to interrogate skull diversity amongst phyllostomid bats, which are adapted to suit a variety of nocturnal dietary habits. By analyzing the timing of skull shape change over the course of embryonic and post‐embryonic development, they show how accelerated growth changes and extended gestation periods contributes to the diversity of bat skull morphologies.…”