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

Background Skull diversity in the neotropical leaf-nosed bats (Phyllostomidae) evolved through a heterochronic process called peramorphosis, with underlying causes varying by subfamily. The nectar-eating (subfamily Glossophaginae) and blood-eating (subfamily Desmondontinae) groups originate from insect-eating ancestors and generate their uniquely shaped faces and skulls by extending the ancestral ontogenetic program, appending new developmental stages and demonstrating peramorphosis by hypermorphosis. However, the fruit-eating phyllostomids (subfamilies Carollinae and Stenodermatinae) adjust their craniofacial development by speeding up certain developmental processes, displaying peramorphosis by acceleration. We hypothesized that these two forms of peramorphosis detected by our morphometric studies could be explained by differential growth and investigated cell proliferation during craniofacial morphogenesis. Results We obtained cranial tissues from four wild-caught bat species representing a range of facial diversity and labeled mitotic cells using immunohistochemistry. During craniofacial development, all bats display a conserved spatiotemporal distribution of proliferative cells with distinguishable zones of elevated mitosis. These areas were identified as modules by the spatial distribution analysis. Ancestral state reconstruction of proliferation rates and patterns in the facial module between species provided support, and a degree of explanation, for the developmental mechanisms underlying the two models of peramorphosis. In the long-faced species, Glossophaga soricina, whose facial shape evolved by hypermorphosis, cell proliferation rate is maintained at lower levels and for a longer period of time compared to the outgroup species Miniopterus natalensis. In both species of studied short-faced fruit bats, Carollia perspicillata and Artibeus jamaicensis, which evolved under the acceleration model, cell proliferation rate is increased compared to the outgroup. Conclusions This is the first study which links differential cellular proliferation and developmental modularity with heterochronic developmental changes, leading to the evolution of adaptive cranial diversity in an important group of mammals

Reproduction of Phylloderma stenops in captivity (Chiroptera, Phyllostomidae)

A reproductive colony of Phylloderma stenops was established in captivity. The bats were maintained in 1/2" wired screen cages sized 90 × 60 × 80 cm in a room with cycles of 13 hours of light and 11 hours of dark and with temperature and humidity ranging from 27 to 31 °C and 75 to 90% respectively. Bats were fed with a semi-liquid diet composed of chopped fruits, raw eggs, bovine meat, dog food, honey, dehydrated shrimp, salt and a vitamin and mineral complex offered daily. In the first two years of confinement the diet was complemented with laboratory-raised cockroaches, mealworms, young mice and seasonal fruits. Nine births occurred from three wild caught females 770-1050 days after capture and two captive-born females. Births occurred in September, February and November-December. The neonate measured 15.0 g of weight and present 34.1 mm of forearm length. Two captive-born females gave birth for the first time at 402-445 days of age. Phylloderma stenops species presents postpartum oestrus, gestation of 5.5 months, lactation of 3.3 months and sexual maturity at 8.0-8.5 months. Fetuses are palpable around two months before birth and females may present synchronisation of births