Exploring the Developmental Origins of Limb Proportion Diversity in Birds: An Analysis of Ontogenetic Timing

Vertebrate limb proportions have diversified in association with species-specific locomotion and life-history strategies. Understanding the ontogenetic origins of this diversity is key to explaining the processes of limb evolution, yet these origins remain poorly investigated. This study explored the developmental timing of limb proportion diversification in birds using published data on limb element lengths (humerus, radius/ulna, femur, and tibiotarsus) at two crucial stages, hatching and adulthood, across 84 species (Wetherbee 1961). We found that while interspecific variation in limb proportions emerges prenatally, these initial patterns further develop into their adult proportions during postnatal growth. Specifically, intralimb stylopod-to-zeugopod ratios slightly decreased or remained constant after hatching, whereas interlimb segmental ratios (i.e., comparisons of homologous elements between the forelimb and hindlimb) changed substantially with the increase in forelimb element lengths. The contribution of prenatal development to limb proportion diversity, as evaluated from the strength of correlation between hatchling and adult proportions, appeared to be comparable among the limb proportion types. However, only for the intra-forelimb proportion, the balance between prenatal and postnatal modification was significantly affected by the developmental mode (precocial, altricial, or intermediate): the correlation was strongest in precocial species and weakest in altricial species, indicating a major contribution from prenatal development and postnatal growth, respectively. These patterns are consistent with the pre- and postnatal ontogenetic trajectory data available for several species, likely reflecting species-specific developmental constraints and postnatal ecological demands. Furthermore, the observed developmental flexibility appeared to be facilitated by a decoupling of postnatal growth between the forelimbs and hindlimbs. Overall, our findings indicate that avian limb proportion variation arises from a variable combination of prenatal patterning and postnatal growth, the balance of which is partly associated with developmental mode. By analyzing an extensive dataset, this study highlights the importance of an ontogenetic perspective for understanding the evolutionary factors driving avian limb diversity.