Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae)

Abstract

The rodent mandible has become a paradigm for studies on the development and evolution of complex morphological structures. We use a combination of geometric and multivariate morphometric methods in order to assess the correspondence between integration patterns and a priori biological models in the context of evolutionary shape divergence in the mandible of rodents of the family Echimyidae. The correlation of shape distances among operational taxonomic units (individuals, species, genera) in separate morphogenetic components allowed the construction of integration matrices among mandible components for data sets corresponding to varying levels of genetic divergence (intergeneric, interspecific, and intrapopulational). The integration matrices were associated with a priori biological (developmental, genetical, modular) models, and the maximum integration axes (singular warps) were compared with realized axes of maximum interspecific variation (relative warps). The integration pattern and intensity were not stable in data sets with different levels of genetic divergence, and the varying functional demands during the ecological radiation in the family were probably responsible for the differences in observed integration patterns. Developmental and genetic models were significantly associated with the interspecific integration patterns observed, suggesting a role for neutral evolution during the evolutionary divergence of mandible shape. However, directional and stabilizing selection were not discarded as processes responsible for the generation of interspecific integration. The choreography of the morphogenetic components in the mandible is highly flexible and the integrated groups of components can be reorganized depending on functional demands during evolutionary shape changes.

Studying morphological integration and modularity at multiple levels: concepts and analysis

“…The advantage of this approach is that specific aspects of variation or covariation can be emphasized, depending on the choice of the analyses. For example, in some structures, the main patterns of overall variation, represented by the shape changes associated with first few principal components, strongly resemble the main patterns of covariation between parts, which can be obtained as the shape changes associated with the first few partial leastsquares axes [10,12,13,16,18,85]. This indicates that the patterns of covariation between parts are also the dominant patterns of overall variation in the structure under study, and therefore emphasize the strength of integration.…”

“…Comparative methods such as independent contrasts or, equivalently, phylogenetic generalized least squares, can be combined with the usual morphometric methods for analysing morphological integration and modularity [18]. This combination of methods has been used in a range of studies, using analyses such as multivariate regressions to estimate evolutionary allometry [18,25,35,92,93], partial leastsquares analysis for examining patterns of integration among parts [16][17][18][19][20][21]26] and tests of modularity [18,21,52].…”

“…Most empirical studies have focused on integration within populations, investigating how the variation among individuals is structured. This is only one aspect of the problem, however, because the concept of integration also applies at different levels [4], including genetic and environmental integration [8,9], integration of fluctuating asymmetry within individuals [9][10][11][12][13][14][15] and evolutionary integration across taxa in a clade [16][17][18][19][20][21]. Most plants, because of their modular body plans, offer additional opportunities to study integration among structures such as leaves or flowers within and among individuals in a population [22,23].…”

“…Most plants, because of their modular body plans, offer additional opportunities to study integration among structures such as leaves or flowers within and among individuals in a population [22,23]. The distinction of different levels makes it possible to compare patterns of integration between them, in order to gain insight into evolutionary and developmental processes from the resemblance of patterns across the levels of integration [8][9][10][11][12]16,[24][25][26][27].…”

Biogeographic variations in wood mice: testing for the role of morphological variation as a line of least resistance to evolution

“…Such methods, based on landmarks or outline analyses, have been used to tackle many topics regarding rodent evolution: evolutionary patterns along fossil lineages (Renaud et al 1996Piras et al 2009;Stoetzel et al 2013), diversification among species, addressing the respective role of adaptation and neutral evolution (e.g. Cardini 2003;Monteiro et al 2005;Macholan 2006;Michaux et al 2007a); differentiation between populations, investigating the role of environmental variations (Renaud 1999;Fadda and Corti 2001;Michaux 2003, 2007;McGuire 2010;Helvaci et al 2012), processes favoring co--occurrence among species , patterns and route of colonization (Valenzuela--Lamas et al 2011;Siahsarvie et al 2012;Cucchi et al 2013). …”