Effect of ancestry on behavioral variation in two species of howler monkeys (Alouatta pigraandA. palliata) and their hybrids

Abstract

Social differences between primate species may result from both flexible responses to current conditions or fixed differences across taxa, yet we know little about the relative importance of these factors. Here, we take advantage of a naturally occurring hybrid zone in Tabasco, Mexico to characterize the variation in social structure among two endangered howler monkey species, Alouatta pigra and A. palliata, and their hybrids. Work in pure populations has suggested that A. pigra females maintain closer proximity, exhibit higher rates of affiliation, and lower rates of agonism than A. palliata females, but we do not know what accounts for this difference. Using identical data collection and analysis methods across three populations, we first seek to confirm previously reported interspecific differences in social structure across all sexes. We next examine: (1) how female social relationships changed with ancestry (by comparing pure and hybrid individuals); (2) how female social relationships changed with group size (A. pigra have smaller groups than A. palliata); and (3) whether female social relationships differed between two taxonomic groups within a single forest fragment (thus controlling for ecological variation). We confirmed previously described species differences, including closer proximity among females than among males in all populations. We also found that smaller groups maintained closer proximity. However, even after accounting for variation in group size, A. pigra females had closer proximity and more affiliation than A. palliata females. Furthermore, differences between pigra-like and palliata-like hybrids paralleled differences between pure populations and persisted even after controlling for ecological variation. Together, our results suggest that flexibility cannot account for all of the social differences between A. pigra and A. palliata and indicate an important genetic component in primate social behavior.

Intragroup genetic relatedness in two howler monkey species (Alouatta pigraandA. palliata): Implications for understanding social systems and dispersal

“…A recent comparative behavioral study by Ho et al [2014] analyzing groups of both species near locations sampled in this study found that A. pigra females were in closer proximity to one another and had higher rates of affiliative behavior than A. palliata females; which ratifies the expected differences based on reports made by numerous behavioral studies on each species [Ho et al, 2014 and references therein]. These differences in social interactions would be expected if within-group A. pigra females were more closely related than A. palliata within-group females, but our study does not provide support for this inference, suggesting that kinship may not always be a strong determinant of social interactions among females.…”

Multiple forms of selection shape reproductive isolation in a primate hybrid zone

“…Here, we examined locus-specific differentiation and introgression using reduced-representation sequencing data from a bimodal howler monkey hybrid zone (Alouatta palliata × Alouatta pigra) (Cortés-Ortiz et al, 2015) and from allopatric parental populations to test predictions about the forms of selection acting on loci associated with reproductive isolation. The parental species diverged ~3 Ma (Cortés-Ortiz et al, 2003) and have many important differences in their morphology (Kelaita, Dias, Aguilar-Cucurachi, Canales-Espinosa, & Cortés-Ortiz, 2011;Smith, 1970), cytogenetics (Steinberg et al, 2008), social systems (Chapman & Balcomb, 1998;Ho et al, 2014) and loud vocalizations (Bergman et al, 2016). Throughout most of their ranges, A. palliata and A. pigra are allopatric, but their ranges overlap in a narrow contact zone (~20 km, Cortés-Ortiz et al, 2007, Cortés-Ortiz et al, 2018 in Tabasco, Mexico (Figure 1).…”

Howler Monkeys

“…Hybrid zones provide the opportunity to explore reproductive strategies of individuals with very different genetic backgrounds (both pure and admixed) in the same ecological and social context (Bergman et al 2008 ). Ongoing studies on the social dynamics in the Mexican hybrid zone (e.g., Ho et al 2014 ) will allow us to evaluate the competitive abilities of hybrid versus purebred individuals. In Brazil, Aguiar ( 2010 ) conducted a study on social interactions in two mixed groups composed of pure A. caraya , A. guariba and putative hybrids.…”

“…Ever since its discovery , research on the anatomical and genetic bases of howler trichromacy has increased. However, the adaptive signifi cance of this trait remains unclear (Hernández- Salazar et al 2014 ). Extensive population-level studies of the distribution of L/M opsin genes and detailed fi eld observations of visual behaviors of howlers are important for elucidating whether trichromacy is related to an enhanced ability to locate orange-and redcolored fruits or young leaves, or to identify changes in the intensity skin and hair pigments as social/reproductive signals Melin et al 2014 ).…”

“…This may not be entirely new, as Alouatta has already served as a model for several theoretical issues in primate evolution, ecology, and behavior, such as the adaptive morphology of the locomotor system and dentition of early catarrhines and Miocene hominoids, the evolution of trichromatic vision, a dissociability model for the study of primate ontogeny, social dynamics and behavioral responses of hybrid populations, the ability to exploit and digest a low quality diet, and the production, propagation, and social function of loud and low amplitude calls Rose 1994 ;Ravosa and Ross 1994 ;Cortés-Ortiz et al 2007 ;Zuñiga Leal and Defl er 2013 ;Ho et al 2014 ;. Chapters in this fi rst volume advance our understanding of howler systematics, evolution, functional anatomy, and physiology and provide new comparative insights into the evolution of howler monkeys within the atelinae.…”