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.
Highlights
Bats (Chiroptera) have a highly specialized postcranial morphology adapted to perform self-powered flight, a trait unique among mammals
This study is the first to demonstrate the presence of fluctuating asymmetry (FA) and directional asymmetry (DA) during bat prenatal development
Our results showed stable magnitudes of longitudinal and cross-sectional FA across prenatal development, rejecting our hypothesis of decreasing asymmetry throughout ontogeny
Summary
Bats (Chiroptera) have a highly specialized postcranial morphology adapted to perform self-powered flight, a trait unique among mammals. Morphological adaptations related to different functional pressures can occur within a single bone (e.g., increased muscle attachment area and biomechanical load resistance in the humerus; Panyutina et al, 2015) Such a variety of long bone adaptations arise ontogenically, mainly through two bone remodeling processes: bone elongation and bone thickening (Enlow, 1963). The former is linked to axial bone deposition via endochondral ossification at growth plates (Webber et al, 2015), whereas the latter results from endosteal and periosteal bone deposition via intramembranous ossification in the periosteum/endosteum (Kronenberg, 2003). Our understanding of the differences in developmental trajectories of bone thickening and elongation in the bat wing remains largely limited
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