Patterns of phenotypic evolution can abruptly shift as species move between adaptive zones. Extant salamanders display three distinct life cycle strategies that range from aquatic to terrestrial (biphasic), to fully aquatic (paedomorphic) and to fully terrestrial (direct development). Life cycle variation is associated with changes in body form such as loss of digits, limb reduction or body elongation. However, the relationships among these traits and life cycle strategy remain unresolved. Here, we use a Bayesian modelling approach to test whether life cycle transitions by salamanders have influenced rates, optima and integration of primary locomotory structures (limbs and trunk). We show that paedomorphic salamanders have elevated rates of limb evolution with optima shifted towards smaller size and fewer digits compared to all other salamanders. Rate of hindlimb digit evolution is shown to decrease in a gradient as life cycles become more terrestrial. Paedomorphs have a higher correlation between hindlimb digit loss and increases in vertebral number, as well as reduced correlations between limb lengths. Our results support the idea that terrestrial plantigrade locomotion constrains limb evolution and, when lifted, leads to higher rates of trait diversification and shifts in optima and integration. The basic tetrapod body form of most salamanders and the independent losses of terrestrial life stages provide an important framework for understanding the evolutionary and developmental mechanisms behind major shifts in ecological zones as seen among early tetrapods during their transition from water to land.
Extant salamanders are used as modern analogs of early digit-bearing tetrapods due to general similarities in morphology and ecology, but the study species have been primarily terrestrial and relatively smaller when the earliest digit-bearing tetrapods were aquatic and an order of magnitude larger. Thus, we created a 3D computational model of underwater walking in extant Japanese giant salamanders (Andrias japonicus) using 3D photogrammetry and open-access graphics software (Blender) to broaden the range of testable hypotheses about the incipient stages of terrestrial locomotion. Our 3D model and software protocol represent the initial stages of an open-access pipeline that could serve as a “one-stop-shop” for studying locomotor function, from creating 3D models to analyzing the mechanics of locomotor gaits. While other pipelines generally require multiple software programs to accomplish the different steps in creating and analyzing computational models of locomotion, our protocol is built entirely within Blender and fully customizable with its Python scripting so users can devote more time to creating and analyzing models instead of navigating the learning curves of several software programs. The main value of our approach is that key kinematic variables (e.g. speed, stride length, and elbow flexion) can be easily altered on the 3D model, allowing scientists to test hypotheses about locomotor function and conduct manipulative experiments (e.g. lengthening bones) that are difficult to perform in vivo. The accurate 3D meshes (and animations) generated through photogrammetry also provide exciting opportunities to expand the abundance and diversity of 3D digital animals available for researchers, educators, artists, conservation biologists, etc. to maximize societal impacts.
more » « less- PAR ID:
- 10535172
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative And Comparative Biology
- ISSN:
- 1540-7063
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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We investigated whether mammals that left terrestrial environments to use air and water as their main locomotor environment experienced constraints on the morphological evolution of their forelimb, assessing their degree of morphological disparity and convergence. We gathered a comprehensive sample of more than 800 species that cover the extant family‐level diversity of mammals, using linear measurements of the forelimb skeleton to determine its shape and size.
Among mammals, fully aquatic groups have the most disparate forelimb shapes, possibly due to the many different functional roles performed by flippers or the relaxation of constraints on within‐flipper bone proportions. Air‐based locomotion, in contrast, is linked to restricted forelimb shape diversity. Bats and gliding mammals exhibit similar morphological patterns that have resulted in partial phenotypic convergence, mostly involving the elongation of the proximal forelimb segments.
Thus, whereas aquatic locomotion drives forelimb shape diversification, aerial locomotion constrains forelimb diversity. These results demonstrate that locomotion in continuous fluid media can either facilitate or limit morphological diversity and more broadly that locomotor environments have fostered the morphological and functional evolution of mammalian forelimbs.
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