Genetic structure of an isolated population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island, Panama

Habitat fragmentation may influence genetic variability through reductions in population size and the physical isolation of conspecifics. We explored the effects of these factors on genetic diversity in a population of mantled howler monkeys (Alouatta palliata) on Barro Colorado Island (BCI), Panama. The study population was established in 1914 when an unknown number of resident individuals were isolated from the surrounding mainland by damming of the Río Chagres to create the Panama Canal. Analyses of 10 microsatellite loci indicated that, despite this isolation, the howler monkeys on BCI exhibit levels of genetic diversity (H _S = 0.584 ± 0.063) among the highest reported for any species of Alouatta. These data also revealed that although relatedness among adults in a social group was significantly greater than zero, the BCI population is not highly genetically structured. Tests for genetic bottlenecks based on departures from equilibrium expectations failed to reveal evidence of a recent reduction in population size. In contrast, coalescent modeling indicated that this population has likely experienced a marked decline within the last few 100 years. These findings generate new insights into the genetic structure of A. palliata and suggest that while the formation of BCI may not have substantially reduced genetic variation in these animals, genetic diversity has been influenced by historical changes in population size.     

The significance of call duration in howler monkeys

The “loud” calls of forest primates consist of repeated sounds that elicit a response from other members of the species. Recent studies suggest that these calls are often displays by the males that permit them to assess the strength of their opponents. Previous research on red howler monkeys supported the hypothesis that howling functions in assessment of competing individuals, as an alternative to energetically expensive chases and fights. As the second step in the attempt to understand the evolution of howling in genus Alouatta,one aspect—call duration — was compared in two species,the mantled howler (Alouatta palliata)and the red howler (A. seniculus).In A. palliatathe median howl duration was 3.5 sec and the interhowl interval was 20.0 sec, while in A. seniculusthe median howl duration was 19.0 sec and the interhowl interval was 3.0 sec. During the dawn chorus, the total duration of calling in A. seniculusmay be 10 or more times greater than that in A. palliata.The latter species appears to be limited in the duration of howls it can produce, so it increases the amount of calling by reducing the interhowl interval. At least four factors may be important in the evolution of the observed differences in call structure: constraints of the acoustic environment, alternate forms of display used by A. palliata,the presence or absence of competing males within the troop, and the effect of female calls on male howling. The observations suggest that the use of the male loud call may reflect differences in the nature of male-male competition and female support more than it reflects the constraints of the acoustic environment.     

Sexual activity of male rhesus monkeys introduced into a heterosexual group.

Unfamiliar males were introduced during the breeding season to a stable heterosexual group of rhesus monkeys to determine how the presence of more dominant resident males affected their mating activity and how their entry was received by resident females. Initially, new males were allowed access to females under controlled conditions both in the presence and absence of resident males, simulating situations which may occur under natural conditions. Results indicated that the sexual activity, including ejaculation rate, of the new males was initially inhibited by the presence of more dominant, resident males, but these inhibiting properties did not carry over to periods when the resident males were absent and were diminished with time. Group females preferentially directed their behavior towards the new males throughout the study. These data suggest that although entry of new males into a stable group is at low rank, their subsequent reproductive success may not be reduced and that the association with resident females may facilitate male rhesus transfer between groups observed during the breeding season.     

Genetic compatibility, mate choice and patterns of parentage: invited review

There is growing interest in the possibility that genetic compatibility may drive mate choice, including gamete choice, particularly from the perspective of understanding why females frequently mate with more than one male. Mate choice for compatibility differs from other forms of choice for genetic benefits (such as 'good genes') because individuals are expected to differ in their mate preferences, changing the evolutionary dynamics of sexual selection. Recent experiments designed to investigate genetic benefits of polyandry suggest that mate choice on the basis of genetic compatibility may be widespread. However, in most systems the mechanisms responsible for variation in compatibility are unknown. We review potential sources of variation in genetic compatibility and whether there is any evidence for mate choice driven by these factors. Selfish genetic elements appear to have the potential to drive mate compatibility mate choice, though as yet there is only one convincing example. There is abundant evidence for assortative mating between populations in hybrid zones, but very few examples where this is clearly a result of selection against mating with genetically less compatible individuals. There are also numerous cases of inbreeding avoidance, but little evidence that mate choice or differential fertilization success driven by genetic compatibility occurs between unrelated individuals. The exceptions to this are a handful of situations where both the alleles causing incompatibility and the alleles involved in mate choice are located in a chromosome region where recombination is suppressed. As yet there are only a few potential sources of genetic compatibility which have clearly been shown to drive mate choice. This may reflect limitations in the potential for the evolution of mate choice for genetic compatibility within populations, although the most promising sources of such incompatibilities have received relatively little research.     

Exploring immature-to-mother social distances in Mexican mantled howler monkeys at Los Tuxtlas, Mexico

We analyzed immature-to-mother social distance (juveniles and non-nursing infants) in two Mexican mantled howler monkey (Alouatta palliata) troops inhabiting a tropical rainforest fragment (40 ha) at Los Tuxtlas, Veracruz, Mexico. During July and August of 2000 and 2001 we applied an instantaneous sampling method (317 hr) to record the behaviors of the immatures and their mothers, as well as distances (ordinal scale) between immatures and their mothers (IMD), and between immatures and nonmother individuals (INMD). Immatures were generally less than 5 m away from any individual of the troop. Social distance was influenced by the different behaviors of both mothers and immatures, with the shortest distances occurring during rest (IMD <5 m in 94% of all instantaneous samples) and the longest during exploration (21% > or =10 m) and play (26% > or =10 m). When IMD increased, we found a higher percentage of records <5 m to other individuals, particularly with the probable father. When the variation in distance to the mother and to other individuals in the troop was considered, the immature animals' distance to other troop members depended on the immatures' age and type of behavior. Overall, these results suggest that in this low-activity species the development of the immature is associated with a complex set of relationships with other troop members.     

Seed predation ofCariniana estrellensis (Lecythidaceae) by black howler monkeys,Alouatta caraya

Seed predation by howler monkeys is poorly documented. Here we report the seed predation onCariniana estrellensis (Lecythidaceae) fruits by the black howler monkeyAlouatta caraya in south-east Brazil during an intense dry season. This observation suggests that even non-specialized seed predators such as howlers can use seeds in critical periods of dry season.     

Testosterone levels of free-ranging resident mantled howler monkey males in relation to the number and density of solitary males: a test of the challenge hypothesis

The challenge hypothesis asserts that testosterone levels and aggression in male adult animals are closely associated with one another in the context of intense reproductive competition, particularly when males challenge one another for the access to females. For mantled howler monkeys (Alouatta palliata), the presence of a solitary male in the vicinity of a social group can be considered a threat for the reproductive success of the resident males, as group takeovers by solitary males are followed by a reestablishment of the access to females among group males and sometimes by infanticide. Therefore, these episodes should be accompanied by an increase in testosterone secretion according to the challenge hypothesis. In order to test our prediction, we relate different group and subpopulation variables to the testosterone levels measured in feces collected from 10 groups living in 6 forest fragments, at Los Tuxtlas, Mexico. Our results suggest that resident A. palliata males regard solitary individuals as potential contesters for their reproductive success and that they respond to interactions with them with an increase in testosterone levels, that is increasing their aggressiveness. Our results also suggest that in the studied groups all males have at least certain access to mates and that the entrance of a new male would affect their reproductive success negatively. Finally, the negative effects of chronically high testosterone levels may be negatively affecting the fitness of our study groups living in high population densities and small fragments.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

Dispersal patterns in Costa Rican mantled howling monkeys

Both male and female juveniles disperse in Costa Rican mantled howling monkeys (Alouatta palliata). 79% of the males and 96% of the females leave their natal groups. Males may spend up to 4 years and females up to 1 year as solitaries. Extra-group individuals are faced with only three possibilities, i.e., form a new group by joining another extra-group individual, join an established social group, or remain solitary. Most surviving extra-group individuals join an established social group which contains no kin. Females join with the help of a resident male and once in a group proceed to rise to the alpha position through dyadic interactions. The immigrant female either becomes the alpha female or leaves and tries again in another group. Males challenge the alpha male and either defeat him or remain solitary. Competition with relatives for limited high quality food may be the reason for both sexes leaving their natal groups in howlers. By leaving, the successful immigrants increase their mothers inclusive fitness while suppressing the fitness of nonrelatives instead of remaining natal and competing with relatives for limited food.     

Survey of Alouatta caraya, the black-and-gold howler monkey, and Alouatta guariba clamitans, the brown howler monkey, in a contact zone, State of Rio Grande do Sul, Brazil: evidence for hybridization

Sympatry and natural hybridization between howler monkey taxa (Alouatta spp.) has only recently being confirmed in the wild. Surveys in areas of potential contact between the distribution of two taxa have shown that sympatry is rare, although more common than previously known. Here we report the results of a survey conducted in a contact zone between the only two sexually dichromatic howler monkey taxa, Alouatta caraya and A. guariba clamitans, in São Francisco de Assis, State of Rio Grande do Sul, Brazil. Our survey, covering an area of about 400 ha at the Cerro dos Negros (29°33′50″–29°35′10″S, 54°58′40″–54°59′50″W; ~100–279 m a.s.l.), was successful in locating seven black-and-gold and one brown howler monkey social groups living syntopically. Black-and-gold group size ranged from 5 to 15 individuals, whereas the brown group was composed of 7 individuals. The pelage color of three adult males belonging to different black-and-gold groups and another adult male belonging to the brown howler group presented a mosaic of red or rufous and black. These adult males and an adult female living in another black-and-gold group are putative hybrids. Therefore, it appears that pre-zygotic reproductive isolation has not evolved, at least not completely, between these howler monkey species, corroborating previous reports for these and other Alouatta taxa. Future genetic studies need to confirm the occurrence of hybridization in this contact zone, and to determine the viability and fertility of hybrids and their possible offspring. In addition, there is no evidence supporting the existence of significant segregation in habitat and resource utilization by black-and-gold and brown howler monkeys.     

Digestive strategies and food choice in mantled howler monkeys Alouatta palliata mexicana: bases of their dietary flexibility

Mantled howler monkeys (Alouatta palliata) occupy a wide variety of tropical habitats and are the most folivorous of New World primates. However, their diet may include fruits, buds, petioles, and flowers, as well as leaves, suggesting they must cope with variations in the nutrient composition of their food. We studied the physiological basis of the dietary flexibility of these monkeys by comparing food choice, digestive performance and patterns of digesta flow in six adults, fed diets of either leaves or a mixture of fruit and leaves. Although monkeys ate similar amounts of the two diets, they ingested more digestible protein when offered the leaf diet, on which they lost body mass, but they ingested much more soluble sugars when offered fruit and leaves on which they gained mass. Digestibilities of dry matter, fat, energy and fibre did not differ between diets, but those of crude protein, soluble sugars and minerals were higher on the fruit–leaf diet. Mean retention times in the gut of solute (Co-EDTA) and particulate markers (Cr-mordanted cell walls) did not differ between diets, but on both diets the monkeys retained the particulate marker (mean retention time ca 55 h) for longer than they did the solute marker (MRT ca 50 h). A lack of selective retention of solutes and small particles in the gastro-intestinal tract of howler monkeys probably restricts them to mixed diets but their digestive strategy is sufficiently flexible to allow them to feed on a diet of leaves when fruit is unavailable.     

Grooming in brown howler monkeys,Alouatta fusca

The grooming behavior of a group of brown howler monkeys was studied for one year in an Atlantic forest reserve of southeastern Brazil. A total of 290 grooming bouts were recorded and analyzed. The two adult females directed most of the grooming (91%), while the adult male was the major recipient (37%). Grooming between females, and between them and their siblings, also occurred quite often. On average, the group spent 2% of its daily time grooming, with a higher frequency around noon. There were significant differences, however, in time spent grooming between seasons; grooming was more abundant during the coldest seasons (autumn–winter) and rarer in hotter ones (spring–summer). A significant negative correlation was found between grooming time and temperature, but contrary to expectations, grooming time failed to correlate with both the group' diet and the demands of food-gathering, as measured by travelling time and day range length. A comparison of grooming behavior with other species of the genus suggests that brown, red (A. seniculus), and black howler monkeys (A. caraya) are more similar to each other than to mantled howlers (A. palliata), a result that probably is linked with the differing social structure and group size of the latter species. © 1995 Wiley-Liss, Inc.     

Anorexia: A “losing” strategy?

Several theorists have tried to model anorexia on Wasser and Barash’s (1983) “reproductive suppression model” (RSM). According to the RSM, individual females adaptively suppress their reproductive functioning under conditions of social or physiological stress. From this perspective, mild anorexia is viewed as an adaptive response to modern conditions; more severe anorexia is viewed as an adaptation gone awry. Previous models have not, however, examined the full richness of the RSM. Specifically, Wasser and Barash documented not only self-imposed reproductive suppression, but also manipulative reproductive suppression of subordinate females by dominants. I propose that the modern “epidemic” of anorexia is explained neither by adaptive self-suppression nor by environmental mismatch (an adaptation gone awry); I propose that the “epidemic” levels of anorexia seen in modern western society are a direct consequence of intrasexual competition, the scope of which has been enhanced by the power and reach of modern communications media. According to this perspective, anorexia, even in its mild forms, is a manipulative strategy imposed on subordinates by dominants. Anorexia is, in both senses, a “losing” strategy. Linda Mealey developed the intrasexual manipulation model of anorexia while on a three-year stint in the psychology department of the University of Queensland; she is currently at the College of St. Benedict in central Minnesota, where she is associate professor of psychology. She is President of the International Society for Human Ethology, a councilor of the Human Behavior and Evolution Society, on the editorial board of Politics and the Life Sciences, and chair of the 1999 and 2000 Aaron Beck New Investigator Award Committee (sponsored by ASCAP: Across Species Comparisons and Psychiatry).     

Primate copulation calls and postcopulatory female choice

Females in some species of Old World monkeys and apes vocalizeafter copulation, but the function of these vocalizations isnot clear. In this article, we examine the hypothesis that copulationcalls are a form of postcopulatory female choice. Accordingto this hypothesis, copulation calls are honest signals of fertility(i.e., ovulation) that are used by females to encourage mateguarding by their preferred mating partners and reduce the likelihoodof sperm competition. Evidence in favor of this hypothesis isreviewed and discussed in relation to other hypotheses. We suggestthat the evolution of female copulation calls in primates islinked to the evolution of other female mating signals suchas exaggerated sexual swellings, the potential for sperm competition,and the opportunity for precopulatory female mate choice.     

Sexual selection and mate choice in evolutionary psychology

The importance of mate choice and sexual selection has been emphasized by the majority of evolutionary psychologists. This paper assesses three cases of work on mate choice and sexual selection in evolutionary psychology: David Buss on cross-cultural human mate preferences, Randy Thornhill and Steve Gangestad on the link between mate preferences and fluctuating asymmetry, and Geoffrey Miller on the role of Fisher’s runaway process in human evolution. A mixture of conceptual and empirical problems in each case highlights the general weakness of work in evolutionary psychology on these issues.

Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice

We studied two multimale–multifemale groups of black howler monkeys (Alouatta pigra) during a 14‐month study (June 2006–July 2007) in Palenque National Park, Mexico to evaluate the ways in which their sexual behavior changes across ovarian cycles. We analyzed 231 fecal samples, collected every 2.2±1.4 days from five females. For four females, estradiol and progesterone profiles revealed an average (±SE) cycle length of 18.3±1.4 days. Copulations occurred significantly more frequently during the periovulatory period (POP), defined as the estimated day of ovulation ±3 days (N=18). This was largely the result of cycling females soliciting sexual interactions during their POPs. Females directed their solicitations significantly more often toward “central” males of their group, who had close spatial associations with females at other times, compared with “noncentral” males, who did not associate closely with females. Central males rarely solicited sexual interactions, but instead monitored the females' reproductive status by sniffing their genitals, and maintained significantly closer proximity to females during their POPs, suggesting male mate guarding when conceptions are most likely to occur. Our findings indicate that the reproductive strategies of black howler central males and females coincide, highly skewing mating opportunities toward central males. Black howler females, however, occasionally choose to copulate with noncentral resident males or extra‐group males during their POPs, undermining the ability of central males to monopolize all reproductive opportunities. Am. J. Primatol. 71:153–164, 2009. © 2008 Wiley‐Liss, Inc.     

Fertilization mode, sperm characteristics, mate choice and parental care patterns in Artedius spp. (Cottidae)

The reproductive biology of three species in the genus Artedius ( A. harringtoni, A. lateralis and A. fenestralis ) was studied, including parental behaviour, mate choice, fertilization mode, gamete morphology and behaviour, and gonad morphology to help understand the coevolution of reproductive characteristics with potentially different modes of fertilization. In all three species, males guard multiple clutches at oviposition sites. In laboratory mate‐choice experiments, males appearred to prefer to defend sites containing eggs and were better able to attract mates at these sites. There was evidence that internal gomete association, although more pronounced in A. harringtoni , existed in all three species. Sperm behaviour and morphology and histological analysis of gonads suggested that A. fenestralis and A. lateralis were more likely to engage in typical external fertilization. The adoption of eggs and their effect on female mate‐choice patterns appearred to reduce the importance of certainty of paternity in these species, and probably increased the evolutionary stability of male parental care.     

Computational mate choice: theory and empirical evidence

The present review is based on the thesis that mate choice results from information-processing mechanisms governed by computational rules and that, to understand how females choose their mates, we should identify which are the sources of information and how they are used to make decisions. We describe mate choice as a three-step computational process and for each step we present theories and review empirical evidence. The first step is a perceptual process. It describes the acquisition of evidence, that is, how females use multiple cues and signals to assign an attractiveness value to prospective mates (the preference function hypothesis). The second step is a decisional process. It describes the construction of the decision variable (DV), which integrates evidence (private information by direct assessment), priors (public information), and value (perceived utility) of prospective mates into a quantity that is used by a decision rule (DR) to produce a choice. We make the assumption that females are optimal Bayesian decision makers and we derive a formal model of DV that can explain the effects of preference functions, mate copying, social context, and females' state and condition on the patterns of mate choice. The third step of mating decision is a deliberative process that depends on the DRs. We identify two main categories of DRs (absolute and comparative rules), and review the normative models of mate sampling tactics associated to them. We highlight the limits of the normative approach and present a class of computational models (sequential-sampling models) that are based on the assumption that DVs accumulate noisy evidence over time until a decision threshold is reached. These models force us to rethink the dichotomy between comparative and absolute decision rules, between discrimination and recognition, and even between rational and irrational choice. Since they have a robust biological basis, we think they may represent a useful theoretical tool for behavioural ecologist interested in integrating proximate and ultimate causes of mate choice.