Are olfactory traits in a pair-bonded primate under sexual selection? An evaluation of sexual dimorphism in Aotus nancymaae.

Whereas the diets of diurnal primate species vary greatly, almost all nocturnal primate species consume insects. Insect-foraging has been described in nocturnal prosimians but has not been investigated in owl monkeys (Aotus spp.). We studied 35 captive owl monkeys (Aotus nancymaae) in order to describe their foraging behavior and to determine if there were any age or sex differences in their ability to capture insect prey. Because owl monkeys cooperate in parental care and in food-sharing, we expected social interactions involving insect prey. We found that owl monkeys most often snatched flying insects from the air and immobilized crawling insects against a substrate using their hands. Immatures and adult female owl monkeys attempted to capture prey significantly more often than did adult males; however, there was no difference in the proportion of attempts that resulted in capture. Social interactions involving prey appeared similar to those with provisioned food, but possessors of prey resisted begging attempts more so than did possessors of other food. Owl monkeys attempted to capture prey often (mean = 9.5 ± 5.8 attempts/h), and we speculate that the protein and lipid content of captured prey is important for meeting the metabolic demands for growth and reproduction.

Sexual Selection and Variance in Reproductive Success

Numerous behavioral studies have shown that animals use olfactory cues as inbreeding avoidance or kin avoidance mechanisms, implying that scent is unique to families. However, few studies have analyzed the chemical profile of a scent and ascertained the messages that are conveyed in scent secretions. Owl monkeys (Aotus nancymaae) are socially monogamous primates that utilize scent when interacting with foreign conspecifics. This suggests there is a difference in the chemical composition of scent marks. We chemically analyzed sub-caudal gland samples from three families of captive owl monkeys (Aotus nancymaae). Samples were analyzed by capillary GC-MS and relative retention time and fragment pattern was compared with known standards. Gland samples were high in large plant-based shikikate metabolites and fatty ketones; alcohols, acids, and acetates were virtually absent. Gender, age, and family could be reliably classified using discriminant analysis (92.9, 100, and 100%, respectively). Female scent profiles were greater in concentration of aromatic plant metabolites, possibly the result of a different diet or physiological differences in female metabolism as compared to male. Offspring of adult age still living in their natal group showed a less complex chemical profile than their parents. Finally, each family had its own unique and complex chemical profile. The presence of family scent may play a role in mediating social interactions.

Broadening our knowledge of olfactory communication in strictly monogamous systems can inform our understanding of how chemosignals may facilitate social and reproductive behavior between the sexes. Compared to other social and mating systems, relatively little is known about olfactory communication in strictly monogamous non-human primates. Furthermore, platyrrhines are not well represented in chemical analyses of glandular secretions. We conducted semi-quantitative headspace gas chromatography with mass spectrometry to investigate the chemical components of glandular secretions from the subcaudal and pectoral glands of a strictly pair-living platyrrhine, the owl monkey (Aotus spp.). In this study, the first chemical analysis of a wild platyrrhine population, our goals were to (1) conduct a robust analysis of glandular secretions from both captive and wild owl monkey populations and (2) identify whether biologically relevant traits are present in glandular secretions. We also compared and contrasted the results between two Aotus species in different environmental contexts: wild Aotus azarae (N = 33) and captive A. nancymaae (N = 104). Our findings indicate that secretions from both populations encode sex, gland of origin, and possibly individual identity. These consistent patterns across species and contexts suggest that secretions may function as chemosignals. Our data also show that wild A. azarae individuals are chemically discriminated by age (adult or subadult). Among the captive A. nanycmaae, we found chemical differences associated with location, possibly caused by dietary differences. However, there was no noticeable effect of contraception on the chemical profiles of females, nor evidence that closely related individuals exhibit more similar chemical profiles in A. nancymaae. Overall, our data suggest that glandular secretions of both wild and captive Aotus convey specific information. Future studies should use behavioral bioassays to evaluate the ability of owl monkeys to detect signals, and consider whether odor may ultimately facilitate social and sexual relationships between male and female owl monkeys.

Chapter 6 - Honey bee pollination ecology

-The mortality of territorial male Red-winged Blackbirds (Agelaius phoeniceus) was determined in a banded population during the breeding seasons of 1973-1978. I used these data to test the hypothesis that sexual selection for characteristics that are advantageous in territory defense or mate acquisition, or both, occurs at the expense of survivorship. Observations of males that returned to the study area to reestablish territories, and of the tenures of these males on their territories, enabled me to partition annual mortality into components that estimate mortality during the and breeding seasons. The mean annual mortality of territorial male Red-wings was 52%, with 29% mortality occurring during the nonbreeding season (1 June to approximately 1 March) and 22% mortality occurring during the breeding season before 1 June. The effect of body size on survivorship was investigated by correlating male wing lengths measured in the third year of life with their ages at death. The correlation between wing length and survivorship was negative (-0.438) and statistically significant (one-tailed P < 0.05). I conclude that mortality during the breeding season is a potentially important selective force in this species, and that sexual selection may have occurred at the expense of survivorship. Sexual selection for large males appears to be opposed by survival selection for small males. Received 13 January 1986, accepted 15 July 1986. DARWIN (1859, 1871) viewed natural and sexual selection as separate but complementary mechanisms of evolution. According to Darwin, natural selection favors adaptations that increase survival, while sexual selection favors adaptations that increase the ability to acquire mates but decrease survival. In contrast, contemporary evolutionary biologists consider both selection for increased survival (survival selection) and selection for increased mating ability (sexual selection) as components of natural selection (see Mayr 1972, Selander 1972). Sexual selection, however, is still thought to occur at the cost of decreased survival (e.g. Selander 1965, Searcy 1979, O'Donald 1980, Lande 1981, Searcy and Yasukawa 1981, Kirkpatrick 1982). Thus, when sexual selection produces sexual dimorphism, the larger and more conspicuous sex is presumed to pay a cost in higher mortality (see Andersson 1982, Searcy and Yasukawa 1983, Payne 1984). Survival selection therefore would act to limit the effects of sexual selection because it would favor smaller, less conspicuous individuals of the sexually selected sex. Although the opposition of sexual and survival selection has been presumed since Darwin (1859), there have been relatively few attempts to document the reduced survival that should accompany sexual selection. The Red-winged Blackbird (Agelaius phoeniceus) is a species in which sexual dimorphism is thought to be the product of sexual selection (see Searcy and Yasukawa 1983). Male Redwings are larger and more conspicuous than are females (Nero 1956a, b; Orians and Christman 1968), and sexual selection is a potentially important evolutionary force because the variance in mating success is high (Payne 1979). However, although sexual selection is thought to act more strongly on male than on female Red-winged Blackbirds (Payne 1979), male and female Red-wing survivorship is virtually identical (Fankhauser 1971, Searcy and Yasukawa 1981). Thus, there is no evidence that males pay a cost in increased mortality. Furthermore, there is little evidence that larger male Red-winged Blackbirds suffer higher mortality than do smaller males (Searcy 1979, Johnson et al. 1980). These observations are inconsistent with the generally accepted view that sexual selection is primarily responsible for the sexual dimorphism in size, plumage, and behavior in Red-winged Blackbirds (see Searcy and Yasukawa 1983). I tested the hypothesis that sexual selection has favored characteristics that enhance a male's ability to acquire a territory or mates, but at the expense of his survival (Selander 1965, Searcy 56 The Auk 104: 56-62. January 1987 This content downloaded from 207.46.13.105 on Wed, 25 May 2016 05:23:12 UTC All use subject to http://about.jstor.org/terms January 1987] Mortality of Male Red-winged Blackbirds 57 1979). This sexual-selection hypothesis predicts that the mortality of males during the breeding season should represent a considerable portion of annual mortality because males pay a cost that results from their conspicuous and energetically expensive attempts to defend their territories and attract mates. I tested this prediction by partitioning the annual mortality of male Red-winged Blackbirds into components that estimate mortality in the breeding and seasons. The hypothesis also predicts that counter-balancing survival selection will favor small males. I tested this prediction by examining the relationship between size and survival of male Red-winged Blackbirds.

Sexual size dimorphism is assumed to be adaptive and is expected to evolve in response to a difference in the net selection pressures on the sexes. Although a demonstration of sexual selection is neither necessary nor sufficient to explain the evolution of sexual size dimorphism, sexual selection is generally assumed to be a major evolutionary force. If contemporary sexual selection is important in the evolution and maintenance of sexual size dimorphism then we expect to see concordance between patterns of sexual selection and patterns of sexual dimorphism. We examined sexual selection in the wild, acting on male body size, and components of body size, in the waterstrider Aquarius remigis, as part of a long term study examining net selection pressures on the two sexes in this species. Selection was estimated on both a daily and annual basis. Since our measure of fitness (mating success) was behavioral, we estimated reliabilities to determine if males perform consistently. Reliabilities were measured as ϰ statistics and range from fair to perfect agreement with substantial agreement overall. We found significant univariate sexual selection favoring larger total length in the first year of our study but not in the second. Multivariate analysis of components of body size revealed that sexual selection for larger males was not acting directly on total length but on genital length. Sexual selection for larger male body size was opposed by direct selection favoring smaller midfemoral lengths. While males of this species are smaller than females, they have longer genital segments and wider forefemora. Patterns of contemporary sexual selection and sexual size dimorphism agree only for genital length. For total length, and all other components of body size examined, contemporary sexual selection was either nonsignificant or opposed the pattern of size dimporhism. Thus, while the net pressures of contemporary selection for the species may still act to maintain sexual size dimorphism, sexual selection alone does not.

Several hypotheses that involve either sexual selection (intra- and intersexual) or disruptive ecological selection (e.g., niche divergence, reproductive role division) or both have been advanced as adaptive explanations for the evolution and maintenance of sexual size dimorphism (SSD). However, ever since Darwin, the prevalent explanation in species with male-biased SSD has been intrasexual selection favoring larger size in males in the competition for mates. Here, I show that in the Galapagos Flightless cormorant (Phalacrocorax harrisi; Phalacrocoracidae), the sexes differ significantly in body mass and in all five external morphometric traits measured, with body mass being the most dimorphic trait followed by bill width and bill depth. Correlations between morphometric traits and between morphometric traits and body mass differed by trait and by sex. Comparative analyses including 16 other species within the family showed that the Flightless cormorant is the largest phalacrocoracid. Several factors are theoretically likely to favor the evolution of larger size and greater SSD in species where the male is larger than the female. However, sexual selection favoring larger size in males through competition for mates or by mate choice all seem unlikely explanations for SSD in the Flightless cormorant. Here, I argue that the main driving force for the evolution of the species’ larger size is disruptive ecological selection involving selection for larger body size in males as an adaptation for larger prey and genetic correlation between the sexes for body size explain the increased size and larger sexual dimorphism of the species. Comparative analyses also showed that the Flightless cormorant has a significantly greater sexual dimorphism in both body mass and bill depth, but dimorphism in bill length was similar to that of other Phalacrocoracidae. Thus, the Flightless cormorant is the most sexually dimorphic of the Phalacrocoracidae. The degree of sexual dimorphism in all traits correlated positively and strongly with mean body mass of each sex and with the mean of both sexes combined. However, the slope of reduced major axis (RMA) regressions of male traits as function of female traits, except for bill depth, did not depart significantly from geometric isometry (β = 1.0), showing that Phalacrocoracidae do not follow Rensch’s rule. Thus, among phalacrocoracids, variation in body size fully explains variation in the degree of interspecific variation in SSD and sexual dimorphism in other traits. This means that a remarkable SSD and sexual dimorphism in other traits in the Flightless cormorant relative to other phalacrocoracids can simply be attributable to the species’ largest size; thus, the magnification of sexual dimorphism, including SSD, is an effect of disruptive ecological selection favoring larger size in males and consequently a lower rate of increase in female size as a correlated response similar to that in other phalacrocoracids resulting from genetic correlation between the sexes for body size. I also suggest that the remarkable larger size (gigantism) and remarkable sexual dimorphism of the Flightless cormorant are both novel character states that have evolved in situ following colonization of the Galapagos Islands.KeywordsFlightless CormorantEcological SelectionSexual Size Dimorphism (SSD)GalapagosBill DepthThese keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male). I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

Mate choice based on body size similarity in sexually dimorphic populations causes strong sexual selection

Nancy Ma's night monkeys (Aotus nancymaae) are significantly impacted by illegal trafficking along the tri-border region between Peru, Colombia, and Brazil. Night monkeys previously used for biomedical research have been released into natural forests along the tri-border region posing a health and conservation threat to local wild monkey populations. We evaluated the health of 55 adult night monkeys during two sampling periods (2018 and 2023) along the tri-border region through clinical evaluation, determination of ectoparasite presence, and through surveillance via PCR of oral swabs and blood samples followed by Sanger sequencing for herpesviruses, orthoflaviviruses, and Mycobacterium tuberculosis complex. Ectoparasites were more commonly found during the dry season (odds ratio=4.18, 95% confidence interval [1.36, 13.99], P=0.015). The presence of herpesvirus and flavivirus was 48.6% (18/37) and 1.8% (1/55), respectively. Sanger sequencing identified two distinct herpesviruses (Aotus nancymaae cytomegalovirus 1 and Aotus nancymaae lymphocryptovirus 1) and one flavivirus (86.18% identity to the Psorophora flavivirus, part of the insect-specific flavivirus lineage II group in South America). Tuberculosis-causing mycobacteria was not detected. Our findings provide molecular evidence that orthoflaviviruses and herpesviruses are detectable in free-ranging night monkeys in the tri-border region, underscoring the importance of future studies to investigate infection dynamics and the prevalence of potential zoonotic pathogens associated with this primate species within the Amazon Basin.

Assessing the long-term macroevolutionary consequences of sexual selection has been hampered by the difficulty of studying this process in the fossil record. Cytheroid ostracodes offer an excellent system to explore sexual selection in the fossil record because their readily fossilized carapaces are sexually dimorphic. Specifically, males are relatively more elongate than females in this superfamily. This sexual shape difference is thought to arise so that males carapaces can accommodate their very large copulatory apparatus, which can account for up to one-third of body volume. Here we test this widely held explanation for sexual dimorphism in cytheroid ostracodes by correlating investment in male genitalia, a trait in which sexual selection is seen as the main evolutionary driver, with sexual dimorphism of carapace in the genus Cyprideis. We analyzed specimens collected in the field (C. salebrosa, USA; C. torosa, UK) and from collections of the National Museum of Natural History, Washington, DC (C. mexicana). We digitized valve outlines in lateral view to obtain measures of size (valve area) and shape (elongation, measured as length to height ratio), and obtained several dimensions from two components of the hemipenis: the muscular basal capsule, which functions as a sperm pump, and the section that includes the intromittent organ (terminal extension). In addition to the assessment of this primary sexual trait, we also quantified two dimensions of the male secondary sexual trait—where the transformed right walking leg functions as a clasping organ during mating. We also measured linear dimensions from four limbs as indicators of overall (soft-part) body size, and assessed allometry of the soft anatomy. We observed significant correlations in males between valve size, but not elongation, and distinct structural parts of the hemipenis, even after accounting for their shared correlation with overall body size. We also found weak but significant positive correlation between valve elongation and the degree of sexual dimorphism of the walking leg, but only in C. torosa. The correlation between the hemipenis parts, especially basal capsule size and male valve size dimorphism suggests that sexual selection on sperm size, quantity, and/or efficiency of transfer may drive sexual size dimorphism in these species, although we cannot exclude other aspects of sexual and natural selection.

In a model group of giant reptiles, we explored the allometric relationships between male and female body size and compared the effects of sexual and fecundity selection, as well as some proximate causes, on macroevolutionary patterns of sexual size dimorphism (SSD). Monitor lizards are a morphologically homogeneous group that has been affected by extreme changes in body size during their evolutionary history, resulting in 14-fold differences among the body sizes of recent species. Here, we analysed data concerning the maximum and/or mean male and female snout—vent lengths in 42 species of monitor lizard from literary sources and supplemented these data with measurements made in zoos. There was a wide scale of SSD from nearly monomorphic species belonging mostly to the subgenus Odatria and Prasinus group of the Euprepriosaurus to apparently male-larger taxa. The variable best explaining SSD was the body size itself; the larger the species, the higher the SSD. This pattern agrees with the currently discussed Rensch's rule, claiming that the relationship between male and female body size is hyperallometric, i.e. the allometric exponent of this relationship exceeds unity and thus SSD increases with body size in the case of male-larger taxa. All our estimates of the reduced major axis regression slopes of this relationship ranged from 1.132 to 1.155. These estimates are significantly higher than unity, and thus unequivocally corroborate the validity of Rensch's rule in this reptilian group. In spite of our expectation that the variation in SSD can be alternatively explained by variables reflecting the strength of sexual selection (presence of male combat), fecundity selection (e.g. clutch size and mass) and/or proximate ecological factors (habitat type), none of these variables had consistent effects on SSD, especially when the data were adjusted to phylogenetic dependence and/or body size.

Nocturnal mammals have unique sensory adaptations to facilitate foraging at night. Owl monkeys (Aotus spp.) are pair-living nocturnal platyrrhines adept at capturing insect prey under low-light conditions. Owl monkeys use acoustic and chemical cues in intraspecific communication and use olfaction to detect fruit as they forage. We conducted an experiment to determine which cues (auditory, olfactory, and visual) Aotus nancymaae rely upon when foraging for insects. We scored the behavior of 23 captive owl monkeys during a series of trials in which monkeys were provided sensory boxes with insect cues either present (experimental box) or absent (control box). Each cue was tested alone and in combination with all other cues (multimodal cues). We used generalized linear mixed models to determine which cues elicited the greatest behavioral response. Owl monkeys approached and spent more time near experimental boxes than control boxes. Male owl monkeys were quicker than their female partners to approach the sensory boxes, suggesting that males may be less neophobic than females. The owl monkeys exhibited behaviors associated with olfaction and foraging (e.g., sneezing, trilling) during trials with multimodal cues and when only olfactory cues were present. When only visual or auditory cues were present, owl monkeys exhibited fewer foraging-related behaviors. After approaching a sensory box, however, they often touched boxes containing visual cues. A. nancymaae may rely on olfactory cues at night to detect a food source from several meters away and then rely more on visual cues once they are closer to the food source. Their use of sensory cues during insect foraging differs from nocturnal strepsirrhines, possibly reflecting physiological constraints associated with phylogeny, given that owl monkeys evolved nocturnality secondarily from a more recent diurnal ancestor.

Primates use different types of vocalizations in a variety of contexts. Some of the most studied types have been the long distance or loud calls. These vocalizations have been associated with mate defense, mate attraction, and resource defense, and it is plausible that sexual selection has played an important role in their evolution. Focusing on identified individuals of known sex and age, we evaluated the sexual dimorphism in a type of loud calls (hoots) in a population of wild owl monkeys (Aotus azarae) in Argentina. We found evidence of sexual dimorphism in call structure, with females and males only emitting one type of call, each differing in dominant frequency and Shannon entropy. In addition, both age-related and sex-specific differences in call usage were also apparent in response to the removal of one group member. Future acoustic data will allow us to assess if there are individual characteristics and if the structure of hoot calls presents differences in relation to the social condition of owl monkeys or specific sex responses to variants of hoot calls' traits. This will provide deeper insights into the evolution of vocal mechanisms regulating pair bonding and mate choice strategies in this and other primate species.