Evolutionary history of quadrupedal walking gaits shows mammalian release from locomotor constraint

Abstract

Vertebrates employ an impressive range of strategies for coordinating their limb movements while walking. Although this gait variation has been quantified and hypotheses for its origins tested in select tetrapod lineages, a comprehensive understanding of gait evolution in a macroevolutionary context is currently lacking. We used freely available internet videos to nearly double the number of species with quantitative gait data, and used phylogenetic comparative methods to test key hypotheses about symmetrical gait origin and evolution. We find strong support for an ancestral lateral-sequence diagonal-couplet gait in quadrupedal gnathostomes, and this mode is remarkably conserved throughout tetrapod phylogeny. Evolutionary rate analyses show that mammals overcame this ancestral constraint, resulting in a greater range of phase values than any other tetrapod lineage. Diagonal-sequence diagonal-couplet gaits are significantly associated with arboreality in mammals, though this relationship is not recovered for other tetrapod lineages. Notably, the lateral-sequence lateral-couplet gait, unique to mammals among extant tetrapods, is not associated with any traditional explanations. The complex drivers of gait diversification in mammals remain unclear, but our analyses suggest that their success was due, in part, to release from a locomotor constraint that has probably persisted in other extant tetrapod lineages for over 375 Myr.

The evolution of asymmetrical gaits in gnathostome vertebrates

“…This result is in concordance with recent analyses that show that the earliest tetrapods (e.g. Ichthyostega) could have moved with a crutching, mudskipper-like asymmetrical gait (Pierce et al, 2012;Molnar et al, 2021) and a modern view that early tetrapods may have used a variety of locomotor modes, including both asymmetrical gaits (Pierce et al, 2013) and symmetrical gaits (Nyakatura et al, 2014;Nyakatura et al, 2019;Wimberly et al, 2021).…”

“…Much of the foundational work on substrate-based gaits suggests that symmetrical gaits are ancestral and asymmetrical gaits are a more derived feature of mammals (de la Croix, 1936;Gambaryan, 1974;Edwards, 1977;Wimberly et al, 2021). Yet, mounting evidence suggests that asymmetrical gaits may not be a recent or uniquely mammalian innovation.…”

Topographically distinct adaptive landscapes for teeth, skeletons, and size explain the adaptive radiation of Carnivora (Mammalia)

“…The post-cranial skeleton therefore tends to exhibit a high degree of inter-element covariance (Young and Hallgrímsson, 2005; Goswami et al, 2009), which may frustrate the production of discontinuous morphological variation that is maximally optimized for a given locomotor demand (Niklas, 1997, 1999, 2004; Marshall, 2014). Scaling of limb proportions in response to changes in body size can also affect functional indices, meaning that more diverse locomotor behaviors can be achieved for a given morphology at small body sizes (Jenkins et al, 1974; Janis and Martín-Serra, 2020; Weaver and Grossnickle, 2020; Wimberly et al, 2021), or that allometric patterns dominate shape change independent of locomotor behavior at larger sizes (Martín-Serra et al, 2014). Finally, while locomotor diversity in Carnivora is striking for a mammalian order, it does not span the full breadth of substrate use, locomotor specialization, or morphological diversity encompassed by sequentially higher-level groupings of mammals, such as Laurasiatheria, Boreoeutheria, or Placentalia, where patterns of shape variation associated with substrate use or behavior may be more discontinuous (Chen and Wilson, 2015; Janis and Martín-Serra, 2020; Weaver and Grossnickle, 2020).…”

Locomotor energetics in the Indonesian blue‐tongued skink (Tiliqua gigas) with implications for the cost of belly‐dragging in early tetrapods

“…The absence of comprehensive fossil material from this transitional period ("Romer's gap"), however, obscures interpretations of how this functional divide was bridged. Early interpretations of gait patterns within stem tetrapods centered around the use of salamander-like gaits, employing either a lateral-sequence walk or an undulating trot in which lateral vertebral movement propelled the animal forward (Edwards, 1977;Faber, 1956;Gray, 1968;Wimberly et al, 2021).…”