Prenatal Developmental Trajectories of Fluctuating Asymmetry in Bat Humeri

Camilo López-Aguirre; Suzanne J Hand; Daisuke Koyabu; Vuong Tan Tu; Laura A B Wilson

doi:10.3389/fcell.2021.639522

Prenatal Developmental Trajectories of Fluctuating Asymmetry in Bat Humeri

Front Cell Dev Biol. 2021 May 26:9:639522. doi: 10.3389/fcell.2021.639522. eCollection 2021.

Authors

Camilo López-Aguirre^{1

2}, Suzanne J Hand², Daisuke Koyabu^{3

4}, Vuong Tan Tu^{5

6}, Laura A B Wilson^{2

7}

Affiliations

¹ Department of Anthropology, University of Toronto Scarborough, Toronto, ON, Canada.
² Earth and Sustainability Science Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia.
³ Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong.
⁴ Research and Development Center for Precision Medicine, University of Tsukuba, Tsukuba, Japan.
⁵ Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Hanoi, Vietnam.
⁶ Graduate University of Science and Technology, Vietnam Academy of Science and Technology, Hanoi, Vietnam.
⁷ School of Archaeology and Anthropology, The Australian National University, Canberra, ACT, Australia.

Abstract

Fluctuating asymmetry (random fluctuations between the left and right sides of the body) has been interpreted as an index to quantify both the developmental instabilities and homeostatic capabilities of organisms, linking the phenotypic and genotypic aspects of morphogenesis. However, studying the ontogenesis of fluctuating asymmetry has been limited to mostly model organisms in postnatal stages, missing prenatal trajectories of asymmetry that could better elucidate decoupled developmental pathways controlling symmetric bone elongation and thickening. In this study, we quantified the presence and magnitude of asymmetry during the prenatal development of bats, focusing on the humerus, a highly specialized bone adapted in bats to perform under multiple functional demands. We deconstructed levels of asymmetry by measuring the longitudinal and cross-sectional asymmetry of the humerus using a combination of linear measurements and geometric morphometrics. We tested the presence of different types of asymmetry and calculated the magnitude of size-controlled fluctuating asymmetry to assess developmental instability. Statistical support for the presence of fluctuating asymmetry was found for both longitudinal and cross-sectional asymmetry, explaining on average 16% of asymmetric variation. Significant directional asymmetry accounted for less than 6.6% of asymmetric variation. Both measures of fluctuating asymmetry remained relatively stable throughout ontogeny, but cross-sectional asymmetry was significantly different across developmental stages. Finally, we did not find a correspondence between developmental patterns of longitudinal and cross-sectional asymmetry, indicating that processes promoting symmetrical bone elongation and thickening work independently. We suggest various functional pressures linked to newborn bats' ecology associated with longitudinal (altricial flight capabilities) and cross-sectional (precocial clinging ability) developmental asymmetry differentially. We hypothesize that stable magnitudes of fluctuating asymmetry across development could indicate the presence of developmental mechanisms buffering developmental instability.

Keywords: Chiroptera; fluctuating asymmetry; humerus; morphogenesis; prenatal development.