Morphogenesis in Bat Wings: Linking Development, Evolution and Ecology

Abstract

The evolution of powered flight in mammals required specific developmental shifts from an ancestral limb morphology to one adapted for flight. Through studies of comparative morphogenesis, investigators have quantified points and rates of divergence providing important insights into how wings evolved in mammals. Herein I compare growth, development and skeletogenesis of forelimbs between bats and the more ancestral state provided by the rat (Rattus norvegicus) and quantify growth trajectories that illustrate morphological divergence both developmentally and evolutionarily. In addition, I discuss how wing shape is controlled during morphogenesis by applying multivariate analyses of wing bones and wing membranes and discuss how flight dynamics are stabilized during flight ontogeny. Further, I discuss the development of flight in bats in relation to the ontogenetic niche and how juveniles effect populational foraging patterns. In addition, I provide a hypothetical ontogenetic landscape model that predicts how and when selection is most intense during juvenile morphogenesis and test this model with data from a population of the little brown bat, Myotis lucifugus.

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

“…Signalling pathways associated with wing membrane morphogenesis (i.e., Fgf10) can also act as regulators of wing muscle and possibly bone growth (Tokita et al, ). Our results for C. sphinx also echo previous findings of differences in the postnatal development of the wing between insectivorous and frugivorous species (Adams, ). Moreover, intraguild differences in postnatal growth have been reported between tropical and temperate insectivorous bat species (Kunz, Adams, & Wood, ).…”

“…Signalling pathways associated with wing membrane morphogenesis (i.e., Fgf10) can also act as regulators of wing muscle and possibly bone growth (Tokita et al, 2012). Our results for C. sphinx also echo previous findings of differences in the postnatal development of the wing between insectivorous and frugivorous species (Adams, 2008).…”

“…With over 1400 living species, bats (order Chiroptera) represent the second largest clade of mammals, and one of the best-known examples of ecomorphological radiation in Mammalia (Bininda-Emonds et al, 2007;Falkowski et al, 2005;Figueirido, Janis, Perez-Claros, De Renzi, & Palmqvist, 2012). Flight was one of the most important evolutionary novelties during this radiation (Adams, 2008;Adams & Shaw, 2013;Arita & Fenton, 1997;Cooper & Tabin, 2008;Cooper et al, 2012). Moreover, bats have evolved behaviors (e.g., terrestrial locomotion) that represent novel functional needs for a flight-adapted postcranium (Hand et al, 2009;Wang et al, 2017).…”

“…However, this conclusion has also been challenged on the basis of developmental data (Nojiri et al, 2018), leaving the question of whether a developmental signal exists in the subordinal divergence in Chiroptera unresolved. Developmental studies in bats have also shown heterochronic acceleration in the development of the foot and thumb compared with other mammals (Koyabu & Son, 2014), the regulatory role that wing membrane has in the development of the wing (Adams, 2008), postnatal compensatory growth between the autopod and zeugopod (Adams, 2008;Adams & Shaw, 2013), and a developmental basis for the diversification of New World leaf-nosed bats (Sears, 2014).…”

Prenatal postcranial development in two species of sympatric Japanese wood mice (<i>Apodemus argenteus</i> and <i>A. speciosus</i>): a comparison of arboreal versus terrestrial congeners

“…Bats’ thumbs are also well developed already at birth and similar in size to those of adults [6]. It is known that their feet and hand thumbs are utilized to tightly grab the mother or cling to the wall of the nursery areas [2, 12, 13]. …”