When size makes a difference: allometry, life-history and morphological evolution of capuchins (Cebus) and squirrels (Saimiri) monkeys (Cebinae, Platyrrhini)

Abstract Background How are morphological evolution and developmental changes related? This rather old and intriguing question had a substantial boost after the 70s within the framework of heterochrony (changes in rates or timing of development) and nowadays has the potential to make another major leap forward through the combination of approaches: molecular biology, developmental experimentation, comparative systematic studies, geometric morphometrics and quantitative genetics. Here I take an integrated approach combining life-history comparative analyses, classical and geometric morphometrics applied to ontogenetic series to understand changes in size and shape which happen during the evolution of two New World Monkeys (NWM) sister genera. Results Cebus and Saimiri share the same basic allometric patterns in skull traits, a result robust to sexual and ontogenetic variation. If adults of both genera are compared in the same scale (discounting size differences) most differences are small and not statistically significant. These results are consistent using both approaches, classical and geometric Morphometrics. Cebus is a genus characterized by a number of peramorphic traits (adult-like) while Saimiri is a genus with paedomorphic (child like) traits. Yet, the whole clade Cebinae is characterized by a unique combination of very high pre-natal growth rates and relatively slow post-natal growth rates when compared to the rest of the NWM. Morphologically Cebinae can be considered paedomorphic in relation to the other NWM. Geometric morphometrics allows the precise separation of absolute size, shape variation associated with size (allometry), and shape variation non-associated with size. Interestingly, and despite the fact that they were extracted as independent factors (principal components), evolutionary allometry (those differences in allometric shape associated with intergeneric differences) and ontogenetic allometry (differences in allometric shape associated with ontogenetic variation within genus) are correlated within these two genera. Furthermore, morphological differences produced along these two axes are quite similar. Cebus and Saimiri are aligned along the same evolutionary allometry and have parallel ontogenetic allometry trajectories. Conclusion The evolution of these two Platyrrhini monkeys is basically due to a size differentiation (and consequently to shape changes associated with size). Many life-history changes are correlated or may be the causal agents in such evolution, such as delayed on-set of reproduction in Cebus and larger neonates in Saimiri.

To those people and institutions who provide generous help and access to the skeletal material: R. Voss and R. MacPhee (American Museum of Natural History); B. Patterson, B. Stanley and L. Heaney (Field Museum of Natural History); L. Salles, J. Oliveira, F. Barbosa and S. Franco (Museu Nacional do Rio de Janeiro); S. Costa and J. de Queiroz (Museu Paraense Emílio Goeldi); M. de Vivo (Museu de Zoologia da Universidade de São Paulo); and R. Thorington and R. Chapman (National Museum of Natural History (USNM, Washington). Many thanks also to Sue Boinski, Jim Cheverud and Sébastien Couette for reading, correcting, and criticizing an earlier version of this manuscript. Of course, as usual, they are not responsible for any error or misinterpretation of any sort on this paper which should all be billed on me. Many thanks also to Felipe Bandoni who help me in digitizing some of the youngs specimens. This research was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), an American Museum of Natural History Collections Study Grant and a Field Musem of Natural History Visiting schoolarship.

To those people and institutions who provide generous help and access to the skeletal material: R. Voss and R. MacPhee (American Museum of Natural History); B. Patterson, B. Stanley and L. Heaney (Field Museum of Natural History); L. Salles, J. Oliveira, F. Barbosa and S. Franco (Museu Nacional do Rio de Janeiro); S. Costa and J. de Queiroz (Museu Paraense Emílio Goeldi); M. de Vivo (Museu de Zoologia da Universidade de São Paulo); and R. Thorington and R. Chapman (National Museum of Natural History (USNM, Washington). Many thanks also to Sue Boinski, Jim Cheverud and Sébastien Couette for reading, correcting, and criticizing an earlier version of this manuscript. Of course, as usual, they are not responsible for any error or misinterpretation of any sort on this paper which should all be billed on me. Many thanks also to Felipe Bandoni who help me in digitizing some of the young's specimens. This research was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), an American Museum of Natural History "Collections Study Grant" and a Field Musem of Natural History "Visiting schoolarship".