Prenatal allometric trajectories and the developmental basis of postcranial phenotypic diversity in bats (Chiroptera)

Abstract

Most morphological and physiological adaptations associated with bat flight are concentrated in the postcranium, reflecting strong functional demands for flight performance. Despite an association between locomotory diversity and trophic differentiation, postcranial morphological diversity in bats remains largely unexplored. Evolutionary developmental biology is a novel approach providing a link between the analysis of genotypic and phenotypic variation resulting from selective pressures. To quantify the morphological diversity of the postcranium in bats and to explore its developmental basis, we reconstructed the postcranial allometric trajectories of nine bat species from different prenatal developmental series, representing five families and both suborders. We tested for allometric growth in Chiroptera and also quantified levels of allometric disparity and inter‐trajectory distances. Using a phylogenetic scaffold, we assessed whether ontogenetic differences reflect evolutionary relationships. We found significant allometric growth trajectories in almost all species. Interspecific trajectory distances showed lower variance within Yinpterochiroptera than within Yangochiroptera and between suborders. Each suborder occupied nonoverlapping sections of allometric space, showing changes in the growth rates of specific bones for each suborder. The allometry‐corrected disparity was significantly higher in larger species. Statistically significant phylogenetic signal in our results suggests that there is an ontogenetic basis for the postcranial morphological diversity in modern bats. Ancestral state reconstruction also showed an increase in the amount of change in shape with size in the larger species studied. We hypothesize that differences in allometric patterns among bat taxa may reflect a size‐dependent evolutionary constraint, whereby variability in body size and allometric patterns are associated.

Phylogeny and foraging behaviour shape modular morphological variation in bat humeri

“…modules of highly correlated traits within a structure) is a major recent development in evolutionary theory (Felice et al, 2018;Gerber, 2013;Klingenberg, 2013). 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).…”

“…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

“…Peaks of longitudinal (stages 2 and 6) and cross-sectional FA (stage 5) at different developmental stages could indicate variations in the timing of ossification onset and/or growth rates across species, following the morphogenetic drift model ( Hallgrímsson, 1998 ). Despite bats showing a general mammalian developmental pattern ( López-Aguirre et al, 2019a ), heterochronies and diverging allometric trajectories for the ossification of the humeri have been found across bat species ( López-Aguirre et al, 2019b ). The reported slower ossification of the humerus in yinpterochiropteran bats could indicate that different growth rates at a given developmental stage could result in increased magnitudes of FA ( López-Aguirre et al, 2019b ).…”

“…Despite bats showing a general mammalian developmental pattern ( López-Aguirre et al, 2019a ), heterochronies and diverging allometric trajectories for the ossification of the humeri have been found across bat species ( López-Aguirre et al, 2019b ). The reported slower ossification of the humerus in yinpterochiropteran bats could indicate that different growth rates at a given developmental stage could result in increased magnitudes of FA ( López-Aguirre et al, 2019b ). However, our study does not allow for the accurate comparison of growth rates across species, reflecting the challenge of amassing embryonic material for non-model species, as not all species have complete developmental series.…”

“…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 ).…”