Postcranial heterochrony, modularity, integration and disparity in the prenatal ossification in bats (Chiroptera)

Abstract

BackgroundSelf-powered flight is one of the most energy-intensive types of locomotion found in vertebrates. It is also associated with a range of extreme morpho-physiological adaptations that evolved independently in three different vertebrate groups. Considering that development acts as a bridge between the genotype and phenotype on which selection acts, studying the ossification of the postcranium can potentially illuminate our understanding of bat flight evolution. However, the ontogenetic basis of vertebrate flight remains largely understudied. Advances in quantitative analysis of sequence heterochrony and morphogenetic growth have created novel approaches to study the developmental basis of diversification and the evolvability of skeletal morphogenesis.Assessing the presence of ontogenetic disparity, integration and modularity from an evolutionary approach allows assessing whether flight may have resulted in evolutionary differences in the magnitude and mode of development in bats.ResultsWe quantitatively compared the prenatal ossification of the postcranium (24 bones) between bats (14 species), non-volant mammals (11 species) and birds (14 species), combining for the first time prenatal sequence heterochrony and developmental growth data. Sequence heterochrony was found across groups, showing that bat postcranial development shares patterns found in other flying vertebrates but also those in non-volant mammals. In bats, modularity was found as an axial-appendicular partition, resembling a mammalian pattern of developmental modularity and suggesting flight did not repattern prenatal postcranial covariance in bats.ConclusionsCombining prenatal data from 14 bat species, this study represents the most comprehensive quantitative analysis of chiropteran ossification to date. Heterochrony between the wing and leg in bats could reflect functional needs of the newborn, rather than ecological aspects of the adult. Bats share similarities with birds in the development of structures involved in flight (i.e. handwing and sternum), suggesting that flight altriciality and early ossification of pedal phalanges and sternum are common across flying vertebrates. These results indicate that the developmental modularity found in bats facilitates intramodular phenotypic diversification of the skeleton. Integration and disparity increased across developmental time in bats. We also found a delay in the ossification of highly adaptable and evolvable regions (e.g. handwing and sternum) that are directly associated with flight performance.Electronic supplementary materialThe online version of this article (10.1186/s12862-019-1396-1) contains supplementary material, which is available to authorized users.

Postnatal development of the largest subterranean mammal (Bathyergus suillus): Morphology, osteogenesis, and modularity of the appendicular skeleton

“…Further research is required to solidify these conclusions, in particular the ossification sequences for the postcranial skeleton requires detailed examination for diverse subterranean species, which will enable comparison with comparative studies of heterochronic shifts in the postcranial skeleton among marsupials and placentals. [106][107][108][109] Other results obtained in this study are the tendency of periosteal modules (bone thickening) to show higher slopes ( Table 5), and that endochondral modules (bone lengthening) showed higher coefficients of determination in comparison to the periosteal modules ( Table 5). It is known that bone length and bone thickness (mineral density) in mammals are regulated by different genes.…”

“…Such differences in intra‐element growth dynamics provide the first insights on the modularity of a single long bone and also explain the heterochronic differences observed between species, which suggest differential adaptive patterns due to phylogenetic and/or developmental constraints. Further research is required to solidify these conclusions, in particular the ossification sequences for the postcranial skeleton requires detailed examination for diverse subterranean species, which will enable comparison with comparative studies of heterochronic shifts in the postcranial skeleton among marsupials and placentals …”

Phylogeny and foraging behaviour shape modular morphological variation in bat humeri

“…Special interest has been taken in studying developmental modularity and how it reflects the evolutionary history of mammals (Goswami et al, 2009;López-Aguirre et al, 2019a;Young et al, 2010).…”

“…Integration and modularity have been shown to either increase or constrain phenotypic variation, shaping evolutionary patterns and ecological adaptations (Felice et al, 2018;López-Aguirre et al, 2019b;Zelditch et al, 2016). GMM and phylogenetic comparative methods have also been applied to study the bat postcranium, revising our understanding of bat postcranial morphology (Louzada et al, 2019), development (López-Aguirre et al, 2019a, 2019b and evolution (López-Aguirre et al, 2019;Stanchak et al, 2019). Prenatal development of the postcranium indicates a positive interaction between integration and disparity across development, while also revealing differences in allometric trajectories between bat suborders (López-Aguirre et al, 2019a, 2019b.…”

Prenatal Developmental Trajectories of Fluctuating Asymmetry in Bat Humeri

“…Uncovering the historical trajectories that led to the morphological diversification and specialization of bats has been greatly limited by a markedly incomplete fossil record ( Brown et al, 2019 ). Evolutionary developmental biology has emerged as a promising approach to study the evolution of bats while circumventing limitations in the fossil record ( Adams, 2008 ; Cooper et al, 2012 ; Camacho et al, 2019 ; López-Aguirre et al, 2019 , a , b ). Studies have provided evidence for the ontogenetic mechanisms behind forelimb specialization in bats and the evolution of vertebrate flight ( Sears et al, 2006 ; Adams, 2008 ; Cretekos et al, 2008 ; Farnum et al, 2008 ; Cooper et al, 2012 ; Adams and Shaw, 2013 ), ecology-driven deviations in chiropteran development from general mammalian patterns, and the phylogenetic signal in postcranial development ( Adams, 1992 ; Koyabu and Son, 2014 ; López-Aguirre et al, 2019 , a , b ).…”