Multilevel assessment of the Lacertid lizard cranial modularity

Abstract

Different factors and processes that produce phenotypic variation at the individual, population, or interspecific level can influence or alter the covariance structure among morphological traits. Therefore, studies of the patterns of integration and modularity at multiple levels—static, ontogenetic, and evolutionary, can provide invaluable data on underlying factors and processes that structured morphological variation, directed, or constrained evolutionary changes. Our dataset, consisting of cranium shape data for 14 lizard species from the family Lacertidae, with substantial samples of hatchlings and adults along with their inferred evolutionary relationships, enabled us to assess modularity and morphological integration at all three levels. Five, not mutually exclusive modularity hypotheses of lizard cranium, were tested, and the effects of allometry on intensity and the pattern of integration and modularity were estimated. We used geometric morphometrics to extract symmetric and asymmetric, as well as allometric and nonallometric, components of shape variation. At the static level, firm confirmation of cranial modularity was found for hypotheses which separate anterior and posterior functional compartments of the skull. At the ontogenetic level, two alternative hypotheses (the “anteroposterior” and “neurodermatocranial” hypotheses) of ventral cranial modularity were confirmed. At the evolutionary level, the “neurodermatocranial” hypothesis was confirmed for the ventral cranium, which is in accordance with the pattern observed at the ontogenetic level. The observed pattern of static modularity could be driven by functional demands and can be regarded as adaptive. Ontogenetic modularity and evolutionary modularity show the same developmental origin, indicating conservatism of modularity patterns driven by developmental constraints.

Ecomorphological diversification in squamates from conserved pattern of cranial integration

“…A squamate-wide pattern seemingly contrasts with a previous study proposing that species of Anolis exhibit different covariation patterns in the skull, particularly within lineages that exhibit more extreme morphologies (14). In addition, the pattern of cranial integration identified here differs from previous analyses with far fewer landmarks and limited to single genus or family (10, 14, 15). Although the pattern within species or genera has not been assessed with comparable high-dimensional morphometric analyses, small-scale variation under localized selection pressures does not contradict large-scale conservation of overall pattern.…”

“…Although size is an important metric, it is only one of many aspects of form, and elucidating the macroevolutionary patterns of such an exceptionally diverse group requires a robust and comprehensive characterization of morphology. Some recent studies have applied landmark-based geometric morphometric (GM) methods to characterize the overall shape of the skull—an information-rich structure to address questions pertaining to the ecological and developmental influences on morphology (10–15). Although they provide important data on shape evolution, these approaches cannot adequately characterize many aspects of skull morphology, as landmarks are generally restricted to sutures and the edges of structures.…”

Cranial integration in the fire salamander, Salamandra salamandra (Caudata: Salamandridae)

“…developmental, genetic), as has been found in compound leaves where development highly modulates any other variation (Klingenberg et al, 2012). Conversely, discrepancy in patterns of integration between evolutionary and static levels have been found in lizards, suggesting that the functional integration pattern at the static level has appeared by adaptation through selection (Urošević et al 2019). Finally, selection can act on any ontogenetic stage and studies have demonstrated that patterns of integration shift through ontogeny (Zelditch, 1988;Zelditch & Carmichael 1989a, 1989bWillmore et al, 2006;Goswami & Polly 2010a;Goswami et al, 2012;Ackermann, 2005).…”

“…In contrast, at the static level, Urošević et al (2012) found that the head of the common lizard (Podarcis muralis) is a highly integrated structure. Patterns of cranial integration across lacertids (lizards) have been found to vary across evolutionary and static levels, with patterns at the evolutionary level more influenced by development and patterns at the static level more influenced by function, which suggests that functional modularity is adaptive and appeared through selection (Urošević et al 2019). In Anolis lizards, patterns of static modularity have also been found to vary across species; a three-module cranial organisation is supported in some Anolis (lizards) species but no support for modular organisation was found in other Anolis species.…”

“…In Anolis lizards, patterns of static modularity have also been found to vary across species; a three-module cranial organisation is supported in some Anolis (lizards) species but no support for modular organisation was found in other Anolis species. Thus, similar to lacertids (Urošević et al, 2019), patterns of cranial integration in Anolis lizards may be evolutionary flexible and influenced by unique functional pressures acting on the diverse cranial shapes (Sanger et al, 2012). Across amniotes, studies of evolutionary and static modularity have therefore recovered a range of modular organisations, from fully integrated to highly modular structures, although differences in results may partially reflect differences in type of data collected Goswami et al, 2019).…”