Ontogenetic allometry and scaling in catarrhine crania

Abstract

In studies of ontogenetic allometry, ontogenetic scaling has often been invoked to explain cranial morphological differences between smaller and larger forms of closely related taxa. These scaled variants in shape have been hypothesized to be the result of the extension or truncation of common growth allometries. In this scenario, change in size is the determining factor, perhaps under direct selection, and changes in cranial shapes are byproducts, not under direct selection themselves. However, many of these conclusions are based on studies that used bivariate generalizations of shape. Even among multivariate analyses of growth allometries, there are discrepancies as to the prevalence of ontogenetic scaling among primates, how shared the trajectories need to be, and which taxa evince properties of scaled variants. In this investigation, we use a large, comparative ontogenetic sample, geometric morphometric methods, and multivariate statistical tests to examine ontogenetic allometry and evaluate if differences in cranial shape among closely related catarrhines of varying sizes are primarily driven by size divergence, that is, ontogenetic scaling. We then evaluate the hypothesis of size as a line of least evolutionary resistance in catarrhine cranial evolution. We found that patterns of ontogenetic allometry vary among taxa, indicating that ontogenetic scaling sensu stricto does not often account for most morphological differences and that large and small taxa within clades are generally not scaled variants. The presence of a variety of ontogenetic pathways for the evolution of cranial shapes provides indirect evidence for selection acting directly on the cranial shape, rather than on size alone.

Comparison of captive and wild fascicularis‐group macaques (Primates, Cercopithecidae) provides insight into cranial form changes in response to rapid environmental changes

“…Variation in cranial form has been hypothesized to initially arise along allometric trajectories by capitalizing on the lability of size as a “line of least evolutionary resistance” (Elton et al, 2010; Marroig & Cheverud, 2005; Ungar & Hlusko, 2016). Shape variation in many clades is strongly influenced by size variation, but studies have also identified unique shape changes independent of allometry that differentiate taxa within a clade (e.g., Cardini & Elton, 2008b; Elton et al, 2010; Frost et al, 2003; Meloro, Cáceres, Carotenuto, Passaro, et al, 2014; Meloro, Cáceres, Carotenuto, Sponchiado, et al, 2014; Perez et al, 2011; Profant, 2002; Simons & Frost, 2020; Singleton, 2002). The geographic shape changes identified here (both on the unadjusted and adjusted Procrustes coordinates) reveal such non‐allometric shapes differentiating fascicularis ‐group species along an approximately latitudinal gradient.…”

“…Estimates of divergence times between subspecies and populations of M. fascicularis in insular southeast Asia are complicated by multiple dispersal events and rapid lineage diversification, but suggest major dispersals occurred ~1.7–0.5 Ma (Evans et al, 2020; Liedigk et al, 2015; Yao et al, 2017). Thus, size could produce rapid morphological changes via developmental plasticity in response to very early populational divergences, but these are followed by the accumulation of evolved non‐allometric shape changes even within 1.5 Ma or less (i.e., between species or higher; Elton et al, 2010; Kuzawa & Thayer, 2011; Perez et al, 2011; Simons & Frost, 2020; Singleton, 2012). These results have implications for understanding how cranial morphology may change in just a few generations in response to rapid environmental change, such as that being experienced globally today.…”

“…How cranial variation arises and evolves is an important question for assessing diversity in cranial morphology across radiations (Cardini & Elton, 2008a, 2008bCardini & Polly, 2013;Elton et al, 2010;Simons & Frost, 2020), with implications for identifying and diagnosing species in the fossil record (Jolly, 1993;Plavcan & Cope, 2001;Wiens, 2004). More recently, studies employing geometric morphometric methods have been able to explore in detail which environmental factors may be influencing cranial morphological variation in primates and to parse geographic patterns of size and shape changes separately (e.g., Buck et al, 2019;Cáceres et al, 2014;Cardini et al, 2007;Cardini & Elton, 2009;Frost et al, 2003;Grunstra et al, 2018;Ito et al, 2014;.…”

“…Examining the ecological and environmental correlates of geographic variation and its role in speciation is a long‐standing endeavor, especially among the widespread and evolutionarily complex cercopithecoid primates (Albrecht & Miller, 1993; Elton, 2007; Elton et al, 2010; Frost et al, 2003; Grunstra et al, 2018; Mayr, 1959). How cranial variation arises and evolves is an important question for assessing diversity in cranial morphology across radiations (Cardini & Elton, 2008a, 2008b; Cardini & Polly, 2013; Elton et al, 2010; Simons & Frost, 2020), with implications for identifying and diagnosing species in the fossil record (Jolly, 1993; Plavcan & Cope, 2001; Wiens, 2004). More recently, studies employing geometric morphometric methods have been able to explore in detail which environmental factors may be influencing cranial morphological variation in primates and to parse geographic patterns of size and shape changes separately (e.g., Buck et al, 2019; Cáceres et al, 2014; Cardini et al, 2007; Cardini & Elton, 2009; Frost et al, 2003; Grunstra et al, 2018; Ito et al, 2014; Meloro, Cáceres, Carotenuto, Passaro, et al, 2014; Meloro, Cáceres, Carotenuto, Sponchiado, et al, 2014).…”

Acis-regulatory sequence of the wing selector gene,vestigial, drives the evolution of scaling relationships inDrosophilaspecies

“…Allometries have been used to analyze morphological changes that give rise to diversity and phenotypic variation in ecology and evolution (Esquerré et al, 2017; Galicia-Mendoza et al, 2021; Gomes Rodrigues et al, 2018; Shingleton, 2010). Depending on how scaling relationships are studied, allometries can be classified as ontogenic (scaling relationships during development and growth within an organism (Esquerré et al, 2017; Simons and Frost, 2021)); static (scaling relationships across a population of organisms in a specific stage of development (Shingleton et al, 2008)), and evolutionary (scaling relationships across individuals of different species (Tidière et al, 2017)). Mathematically, the scaling of any two traits or characters x and y within an organism can be modeled using the growth law: where a (known as the allometry coefficient) and b are parameters that are fitted to data measurements of ( x, y ) pairs.…”