Insights into Reproductive Strategies and Sexual Selection in Howler Monkeys

Abstract

The genus Alouatta is characterized by a fl exible social system in which the reproductive strategies of males and females show great variability both within and between species. Even though the mating system of some species is more frequently polygynous (e.g., A. arctoidea , A. seniculus, and A. pigra ) and that of other species more often polygynandrous (e.g., A. caraya and A. palliata ), females in all species whose reproductive behavior has been studied have been reported to copulate with multiple males within their group, with males in neighboring groups, and with solitary males, suggesting a "mixed mating strategy" characterized by periods of selective mating and periods of promiscuous mating. Central males, however, may be able to monopolize most breeding opportunities during the periovulatory period (POP) of the ovarian cycle when conception is most likely to occur by forming consortships with cycling females. Females do not avoid these consortships as they sexually solicit the central male frequently during their POPs. All howler monkey species are sexually dimorphic in body size, canine size, and hyoid apparatus, suggesting high male-male competition. In addition, four taxa present degrees of sexual dichromatism. Infanticide has been observed in various howler monkey species and might play an important role in shaping their social systems. We review the reproductive behavior of Alouatta , discuss male and female reproductive strategies that are associated with sexual selection via intrasexual selection, mate choice, or intersexual confl ict, and propose a model for the evolution of reproductive behavior in atelid primates.Resumen El género Alouatta se caracteriza por un sistema social fl exible en cual las estrategias reproductivas de los machos y las hembras muestran una gran vari-

Endocrinology of Howler Monkeys: Review and Directions for Future Research

“…Although a limited number of studies of howler monkeys have focused on ovarian cycles, the effects of male-male competition, fruit availability, fragmentation, and translocation, information is extremely limited on hormonal profi les during infant development, the onset of sexual maturation, pregnancy, and patterns of hormonal fl uctuation in response to seasonal changes in food availability across disturbed and undisturbed habitats. In addition, endocrine studies exploring the nature and formation of social bonding among male-male coalitions, mother-offspring bonds, or the role of paternal care during infant social development focusing on peptide hormones like oxytocin, prolactin, and vasopressin (e.g., Schradin and Anzenberger 2004 ;Seltzer and Ziegler 2007 ;Ziegler et al 2009b ;Anestis 2010 ;Moscovice and Ziegler 2012 ) are needed, especially in order to compare differences between howler groups or species in which collective action, male-male tolerance, and female-female tolerance, and female mate choice have been reported (Pope 1990(Pope , 2000Van Belle et al 2008, b , 2011Kowalewski and Garber 2010 ;Garber and Kowalewski 2011 ).…”

“…For example, endocrine studies have suggested a nonaggressive form of intragroup male-male competition over access to fertile females in black howler monkeys based on elevated androgen and glucocorticoid levels in central compared to noncentral males , despite otherwise neutral male-male social relationships based on tolerance and avoidance (Van Belle et al 2008 ). A direct relationship between male steroid levels and male-female social and sexual interactions also has been observed in tufted capuchin monkeys (Lynch et al 2002 ), Japanese macaques ( Macaca fuscata , Barrett et al 2002 ), and bonobos ( Pan paniscus , Surbeck et al 2012 ), suggesting that social relationships of males with cycling females may be a more pervasive driver of male endocrine function than generally thought.…”

“…These included (1) three take-over events during which three coalitions of two extragroup males each took over one of the study groups and evicted all adult resident males ( N = 2 males per event) and (2) three male immigration events during which a single extragroup male joined either of the two study groups that had one, two, or three resident males at the time of immigration. This did not result in the eviction of resident males, except for one case in which one of the three adult resident males was evicted (for more details see Van Belle et al 2008 ). Immigrant males ( N = 9) had no signifi cant differences in their fecal glucocorticoid and androgen levels during week 1 and week 2 following the take-over/immigration compared to week 3 and week 4.…”

“…palliata : Clarke 1983 ;Glander 1992 ;Dias et al 2010 ;A. pigra : Horwich et al 2000 ;Van Belle et al 2008 ;A. seniculus : Izawa and Lozano 1991 ;Kimura 1992 ;Izawa 1997 ).…”

“…Although, resident black howler males seldom engaged in intrasexual agonistic (mean rate = 0.007 interactions/h/dyad) or affi liative interactions (mean rate = 0.009 interactions/h/dyad) and no agonistic dominance hierarchy could be discerned (Van Belle et al 2008 ), one resident adult male per group, referred to as the "central" male, was found to monopolize almost all mating opportunities, spent signifi cantly more time in close proximity to females, and engaged in affi liation at signifi cantly higher rates with cycling females than did "noncentral" males . Noncentral males had very limited mating opportunities and accounted for only 4 % of copulations (Van Belle et al 2008 ). In addition, central males had signifi cantly higher fecal androgen and glucocorticoid levels compared to noncentral males, suggesting that their efforts of fostering social relationships with females might represent a nonaggressive form of male-male competition over sexual access to females.…”