Early diversification of avian limb morphology and the role of modularity in the locomotor evolution of crown birds

Abstract

High disparity among avian forelimb and hind limb segments in crown birds relative to non-avialan theropod dinosaurs, potentially driven by the origin of separate forelimb and hind limb locomotor modules, has been linked to the evolution of diverse avian locomotor behaviors. However, this hypothesized relationship has rarely been quantitatively investigated in a phylogenetic framework. We assessed the relationship between the evolution of limb morphology and locomotor behavior by comparing a numerical proxy for locomotor disparity to morphospace sizes derived from a dataset of 1,241 extant species. We then estimated how limb disparity accumulated during the crown avian radiation. Lastly, we tested whether limb segments evolved independently between each limb module using phylogenetically informed regressions. Hind limb disparity increased significantly with locomotor disparity after accounting for clade age and species richness. We found that forelimb disparity accumulated rapidly early in avian evolution, whereas hind limb disparity accumulated later, in more recent divergences. We recovered little support for strong correlations between forelimb and hind limb morphology. We posit that these findings support independent evolution of locomotor modules that enabled the striking morphological and behavioral disparity of extant birds.

Morphological Covariance and Onset of Foot Prehensility as Indicators of Integrated Evolutionary Dynamics in the Herons (Ardeidae)

“…As in our study, Stoessel et al. (2013) found a positive correlation between tibiotarsus and tarsometatarsus lengths among 236 species of birds sampled across all major avian subclades, but an “inverse proportionality” between the femur and tarsometatarsus (as also stated for flamingos by Eliason et al. 2023 , p. 348); notably, in addition, an inverse proportional covariation between the femur and tibiotarsus was determined only in “rather long-legged birds” (p. 489), as our data indicate for 24 heron taxa.…”

“…Larger (heavier) heron species have larger heads and longer legs (all P < 0.001, Table 4 ); significant correlation between avian body mass and limb measurements is expected ( Eliason et al. 2023 ).…”

“…And finally, why test for covariance and potential morphological trade-offs specifically between the limb module and the cranium module? More typically, comparisons are made between/among avian “locomotor modules,” such as the forelimbs, hind limbs, and tail (e.g., Gatesy and Dial 1996 ; Eliason et al. 2023 ).…”

A surrogate forelimb: Evolution, function and development of the avian cervical spine

“…Changes to patterns of integration and modularity over evolutionary timescales can influence the macroevolutionary dynamics of a clade (Goswami et al, 2014). Integration and modularity are key components of avian evolution, as the shift from two locomotor modules (forelimb and hindlimb+tail) to three (forelimb, hindlimb, tail) across the dinosaur-bird transition contributed to the evolution of powered flight (Clarke & Middleton, 2008;Eliason et al, 2023;Gatesy & Dial, 1996). Following this, a decrease of integration between the fore-and hindlimbs allowed for a dramatic increase in locomotor behaviour disparity in extant birds (Eliason et al, 2023).…”

“…By synthesizing almost a century's worth of this work during this review (Boas, 1929;Eliason et al, 2023), it is apparent that although we understand the fundamental principles of neck development, function and evolution in birds there is still much work to be done.…”