Diversification of the ruminant skull along an evolutionary line of least resistance

Abstract

Clarifying how microevolutionary processes scale to macroevolutionary patterns is a fundamental goal in evolutionary biology, but these analyses, requiring comparative datasets of population-level variation, are limited. By analyzing a previously published dataset of 2859 ruminant crania, we find that variation within and between ruminant species is biased by a highly conserved mammalian-wide allometric pattern, CREA (craniofacial evolutionary allometry), where larger species have proportionally longer faces. Species with higher morphological integration and species more biased toward CREA have diverged farther from their ancestors, and Ruminantia as a clade diversified farther than expected in the direction of CREA. Our analyses indicate that CREA acts as an evolutionary “line of least resistance” and facilitates morphological diversification due to its alignment with the browser-grazer continuum. Together, our results demonstrate that constraints at the population level can produce highly directional patterns of phenotypic evolution at the macroevolutionary scale. Further research is needed to explore how CREA has been exploited in other mammalian clades.

Developmental origin underlies evolutionary rate variation across the placental skull

“…Developmental origin is of course not the only factor impacting macroevolutionary trajectories of cranial regions. Size and phylogeny have long been identified as primary factors impacting skull evolution [23,[112][113][114][115][116][117][118], and both are significantly associated with variation in shape for each cranial region studied here. Nonetheless, there is substantial range in their effects across the cranium, as may be expected given the potentially competing functions and pressures experienced by different cranial regions [4,73,105,112,113].…”

“…However, non-whale aquatic mammals, including piscivorous pinnipeds also show shifts in their nares, rostrums and palates, associated with respiration, sexual dimorphism and feeding behaviour [72]. Herbivores show the fastest rates of evolution in anterior face and zygomatic region, reflecting elongation of the face and modification of the premaxilla for either evergrowing incisors or entire loss of these teeth [146,[149][150][151][152], as well as presence of a complete postorbital bar in many herbivores, such as equids, some artiodactyls, and primates [116,135,149]. By contrast, carnivores show the fastest evolution for the midface and vault, with the latter potentially reflecting increased attachment area for the temporalis muscle [73,102,137,138,[153][154][155].…”

Functionally mediated cranial allometry evidenced in a genus of rock-wallabies

“…Aside from this developmental pattern, cranial shape variation within the genus appears to be dominated by changes to biomechanical attributes, whose relations to biting ability are well-known among mammals. We found projected premaxillae in larger species, as is typical in extant mammalian herbivores [ 8 , 13 , 17 – 19 , 52 ] and indicative of poorer leverage when biting with the anterior dentition [ 16 , 53 , 54 ]. This also occurred alongside more anterior positioning of the entire functional cheek tooth row and a relatively gracile rear zygomatic arch, reflecting our hypothesized attributes for larger species.…”

“…Conversely, the cranium of the smaller species is likely to reflect a functional emphasis on bite force capacity in their cranial morphology [8]. This 'bite force allometry' is especially clear across extant mammalian herbivores, evidenced by the longer, more gracile skulls of larger species [8,13,[16][17][18][19], and is likely to be a major influence on mammalian cranial diversity in general [8]. However, ontogenetic, static and evolutionary allometry are often correlated and not easily distinguished from each other [8], potentially leading to some functional aspects of morphology being missed through the dismissal of allometry as a determinant of function in morphological studies.…”

Distribution theories for genetic line of least resistance and evolvability measures

“…There have been criticisms and caveats from various standpoints over this research program, including its blindness to mechanistic basis, simplistic assumptions, and uncertainty in the stability of G over pertinent timescales (Pigliucci, 2006; Morrissey et al ., 2010; Milocco & Salazar-Ciudad, 2020, 2022; Henry & Stinchcombe, 2023b). Nevertheless, active research effort exemplifies persistent interest in understanding potential roles of constraints in macroevolutionary phenotypic diversification (Polly & Mock, 2018; Watanabe, 2018; Machado, 2020; Renaud et al ., 2021; Rhoda et al ., 2023). In addition, recent meta-analyses have demonstrated that the amount of evolvability available to selection can roughly predict that of phenotypic divergence (Opedal et al ., 2023; Voje et al ., 2023).…”