Ecogeographical variation in skull shape of capuchin monkeys

Abstract

Aim Because of their recent evolutionary radiation, capuchin monkeys represent an ideal group with which to investigate ecomorphological adaptations in relation to geography and climate. Our aim was to identify patterns of both skull size and shape variation in capuchins in relation to environmental variables and latitude.Location Tropical and subtropical South America.Methods We performed geometric morphometric analyses of skull shape in 228 capuchin monkey individuals belonging to either the genera Sapajus (seven species) or Cebus (two species), representing 94 localities in South America. Twenty-three homologous landmarks were digitized to describe skull shape. We regressed skull shape against latitude, longitude, skull size and environmental variables, using ordinary and partial least squares regressions. Variation partitioning was used to test for the relative contribution to shape variance by taxonomy, allometry and environment, and their interaction terms. ResultsWe found a significant impact of latitude, climate and size on skull shape. The allometric component of shape variation, although large, is not congruent with shape differences between species, and probably reflects ontogenetic effects. Partial least squares between bioclimatic variables and skull shape explain some 98% of the covariation between environment and shape. Species distributed in drier, more seasonal southern localities exhibit a narrow skull with elongated muzzle and relatively larger teeth. Variation partitioning suggests that the difference in skull shape between species is highly correlated with climatic variation but not with skull size.Main conclusions Skull shape in capuchins is significantly related to both environment and skull size. The former, but not the latter, is significantly associated with shape differences between species. The Sapajus clade originated in the south, and experienced an evolutionary radiation during the Pleistocene. As new Sapajus species moved to the north, they adapted to the local environmental conditions, eventually resembling Cebus in skull shape as they reached the Amazon rain forest, in response to their shared environmental conditions.

Checklist of mammals from Mato Grosso do Sul, Brazil

“…Among primates, Sapajus seems to be represented by two species, considering the presumable occurrence of Sapajus libidinosus in the northeastern portion of the state. This species is well known to occur at Emas National Park and it is distributed along a diagonal gradient from northeastern to central Brazil (Lynch Alfaro et al, 2011;Cáceres et al, 2015). There is no reason for its absence in the northeastern region of the Mato Grosso do Sul, as a portion of the Emas National Park is within the state.…”

Geometric morphometrics meets metacommunity ecology: environment and lineage distribution affects spatial variation in shape

“…Variables were selected based on intraspecific and crossspecies studies that showed these variables are correlated with skull and mandible shape variation in mammals (temperature and temperature seasonality: Martínez and Cola 2011, Cáceres et al 2014, Martínez et al 2014, Meloro et al 2014elevation: Alvarado-Serrano et al 2013, primary productivity: Cardini et al 2007; land cover or vegetation type: Monteiro et al 2003, Alvarado-Serrano et al 2013). Variables were selected based on intraspecific and crossspecies studies that showed these variables are correlated with skull and mandible shape variation in mammals (temperature and temperature seasonality: Martínez and Cola 2011, Cáceres et al 2014, Martínez et al 2014, Meloro et al 2014elevation: Alvarado-Serrano et al 2013, primary productivity: Cardini et al 2007; land cover or vegetation type: Monteiro et al 2003, Alvarado-Serrano et al 2013).…”

“…Myriad studies have shown that shape variation follows environmental gradients. Climatic factors explain the skull shape variation of several species of capuchin monkeys (Cáceres et al 2014) and Graomys (Martínez and Cola 2011) across South America. Climatic factors explain the skull shape variation of several species of capuchin monkeys (Cáceres et al 2014) and Graomys (Martínez and Cola 2011) across South America.…”

Environment and space as drivers of variation in skull shape in two widely distributed South-American Tayassuidae,Pecari tajacuandTayassu pecari(Mammalia: Cetartiodactyla)

“…Despite the vast literature (Cardini et al ., ; Cáceres et al ., ; Meloro et al ., , b; Bubadué et al ., ), geographic variation in mammalian skulls has been poorly explored for some groups such as ungulates (although some information is available for Suiformes). Endo et al .…”

“…In this respect, morphological variation across the environmental gradient might reflect not only evolutionary adaptations, but also the phenotypic plasticity of species (Peres‐Neto & Magnan, ; Souto‐Lima & Millien, ; Jaffe, Campbell‐Staton & Losos, ). Most life history traits often covary with size (Gould, ), even across large spatial scales (Cáceres et al ., ; Meloro et al ., , b). For instance, in Old and New World primates and carnivores, differences in skull size have produced new skull size–shape associations and consequent diversification in the diet (Marroig & Cheverud, ; Singleton, ; Meloro et al ., ).…”