Muhammad Agil

Mitochondrial evidence for multiple radiations in the evolutionary history of small apes

BackgroundGibbons or small apes inhabit tropical and subtropical rain forests in Southeast Asia and adjacent regions, and are, next to great apes, our closest living relatives. With up to 16 species, gibbons form the most diverse group of living hominoids, but the number of taxa, their phylogenetic relationships and their phylogeography is controversial. To further the discussion of these issues we analyzed the complete mitochondrial cytochrome b gene from 85 individuals representing all gibbon species, including most subspecies.ResultsBased on phylogenetic tree reconstructions, several monophyletic clades were detected, corresponding to genera, species and subspecies. A significantly supported branching pattern was obtained for members of the genus Nomascus but not for the genus Hylobates. The phylogenetic relationships among the four genera were also not well resolved. Nevertheless, the new data permitted the estimation of divergence ages for all taxa for the first time and showed that most lineages emerged during four short time periods. In the first, between ~6.7 and ~8.3 mya, the four gibbon genera diverged from each other. In the second (~3.0 - ~3.9 mya) and in the third period (~1.3 - ~1.8 mya), Hylobates and Hoolock differentiated. Finally, between ~0.5 and ~1.1 mya, Hylobates lar diverged into subspecies. In contrast, differentiation of Nomascus into species and subspecies was a continuous and prolonged process lasting from ~4.2 until ~0.4 mya.ConclusionsAlthough relationships among gibbon taxa on various levels remain unresolved, the present study provides a more complete view of the evolutionary and biogeographic history of the hylobatid family, and a more solid genetic basis for the taxonomic classification of the surviving taxa. We also show that mtDNA constitutes a useful marker for the accurate identification of individual gibbons, a tool which is urgently required to locate hunting hotspots and select individuals for captive breeding programs. Further studies including nuclear sequence data are necessary to completely understand the phylogeny and phylogeography of gibbons.

Sexual signalling in female crested macaques and the evolution of primate fertility signals

BackgroundFemale signals of fertility have evolved in diverse taxa. Among the most interesting study systems are those of multimale multifemale group-living primates, where females signal fertility to males through multiple signals, and in which there is substantial inter-specific variation in the composition and reliability of such signals. Among the macaques, some species display reliable behavioural and/or anogenital signals while others do not. One cause of this variation may be differences in male competitive regimes: some species show marked sexual dimorphism and reproductive skew, with males fighting for dominance, while others show low dimorphism and skew, with males queuing for dominance. As such, there is variation in the extent to which rank is a reliable proxy for male competitiveness, which may affect the extent to which it is in females’ interest to signal ovulation reliably. However, data on ovulatory signals are absent from species at one end of the macaque continuum, where selection has led to high sexual dimorphism and male reproductive skew. Here we present data from 31 cycles of 19 wild female crested macaques, a highly sexually dimorphic species with strong mating skew. We collected measures of ovarian hormone data from faeces, sexual swelling size from digital images, and male and female behaviour.ResultsWe show that both sexual swelling size and female proceptivity are graded-signals, but relatively reliable indicators of ovulation, with swelling size largest and female proceptive behaviours most frequent around ovulation. Sexual swelling size was also larger in conceptive cycles. Male mating behaviour was well timed to female ovulation, suggesting that males had accurate information about this.ConclusionThough probabilistic, crested macaque ovulatory signals are relatively reliable. We argue that in species where males fight over dominance, male dominance rank is surrogate for competitiveness. Under these circumstances it is in the interest of females to increase paternity concentration and assurance in dominants beyond levels seen in species where such competition is less marked. As such, we suggest that it may in part be variation in male competitive regimes that leads to the evolution of fertility signalling systems of different reliability.

Social tolerance in wild female crested macaques (Macaca nigra) in Tangkoko-Batuangus Nature Reserve, Sulawesi, Indonesia.

In primates, females typically drive the evolution of the social system and present a wide diversity of social structures. To understand this diversity, it is necessary to document the consistency and/or flexibility of female social structures across and within species, contexts, and environments. Macaques (Macaca sp.) are an ideal taxon for such comparative study, showing both consistency and variation in their social relations. Their social styles, constituting robust sets of social traits, can be classified in four grades, from despotic to tolerant. However, tolerant species are still understudied, especially in the wild. To foster our understanding of tolerant societies and to assess the validity of the concept of social style, we studied female crested macaques, Macaca nigra, under entirely natural conditions. We assessed their degree of social tolerance by analyzing the frequency, intensity, and distribution of agonistic and affiliative behaviors, their dominance gradient, their bared‐teeth display, and their level of conciliatory tendency. We also analyzed previously undocumented behavioral patterns in grade 4 macaques: reaction upon approach and distribution of affiliative behavior across partners. We compared the observed patterns to data from other populations of grade 4 macaques and from species of other grades. Overall, female crested macaques expressed a tolerant social style, with low intensity, frequently bidirectional, and reconciled conflicts. Dominance asymmetry was moderate, associated with an affiliative bared‐teeth display. Females greatly tolerated one another in close proximity. The observed patterns matched the profile of other tolerant macaques and were outside the range of patterns of more despotic species. This study is the first comprehensive analysis of females’ social behavior in a tolerant macaque species under natural conditions and as such, contributes to a better understanding of macaque societies. It also highlights the relevance of the social style concept in the assessment of the degree of tolerance/despotism in social systems. Am. J. Primatol. 75:361‐375, 2013.

Mate-guarding constrains feeding activity but not energetic status of wild male long-tailed macaques (Macaca fascicularis)

Mate-guarding is an important determinant of male reproductive success in a number of species. Little is known however about the constraints of this behaviour, e.g. the associated energetic costs. We investigated these costs in long-tailed macaques where alpha males mate guard females to a lesser extent than predicted by the priority of access model. The study was carried out during two mating periods on three wild groups living in the Gunung Leuser National Park, Indonesia. We combined behavioural observations on males’ locomotion and feeding activity, GPS records of distance travelled and non-invasive measurements of urinary C-peptide (UCP), a physiological indicator of male energetic status. Mate-guarding led to a decrease in feeding time and fruit consumption suggesting a reduced intake of energy. At the same time, vertical locomotion was reduced, which potentially saved energy. These findings, together with the fact that we did not find an effect of mate-guarding on UCP levels, suggest that energy intake and expenditure was balanced during mate-guarding in our study males. Mate-guarding thus seems to not be energetically costly under all circumstances. Given that in strictly seasonal rhesus macaques, high-ranking males lose physical condition over the mating period, we hypothesise that the energetic costs of mate-guarding vary inter-specifically depending on the degree of seasonality and that males of non-strictly seasonal species might be better adapted to maintain balanced energetic condition year-round. Finally, our results illustrate the importance of combining behavioural assessments of both energy intake and expenditure with physiological measures when investigating energetic costs of behavioural strategies.

Multicomponent and multimodal lipsmacking in crested macaques (Macaca nigra)

Primates’ communicative signals are often dynamic and composed of multiple components, sometimes belonging to different sensory modalities. Such multicomponent signals are of crucial importance in the study of communication: the addition of extra features to a signal has the potential to modulate or change the meaning and message of the specific signal. Traditionally, however, components of compound signals are studied in isolation from each other, or communicative displays are studied as static and invariant wholes. Both approaches may not allow us to assess the full function of the signals. In crested macaques (Macaca nigra), the lipsmack (a display mainly used in affiliative interactions) can be produced alone or combined with other visual and acoustic communicative features. We investigated whether the composition of the lipsmack influenced the outcome of social interaction while controlling for relationship quality. Our results show that lipsmacks composed of both visual and vocal components (i.e. multimodal signals) increased the probability of affiliative contact, and therefore have enhanced signal value. The total number of visual components involved in the display had no effect but some visual components seemed more influential than others. By analyzing lipsmacking behavior as a composite, dynamic display, we were able to reveal a level of complexity that is not apparent when looking at each component separately. The results highlight the importance of a more integrative, multimodal approach to the study of primate communication. Am. J. Primatol. 75:763–773, 2013.

Costs of mate-guarding in wild male long-tailed macaques (Macaca fascicularis): Physiological stress and aggression

Mate-guarding is an important determinant of male reproductive success in a number of species. However, it is known to potentially incur costs. The aim of the present study was to assess the effect of mate-guarding on male physiological stress and aggression in long-tailed macaques, a species in which males mate-guard females to a lesser extent than predicted by the Priority of Access model (PoA). The study was carried out during two mating periods on three groups of wild long-tailed macaques in Indonesia by combining behavioral observations with non-invasive measurements of fecal glucocorticoid (fGC) levels. Mate-guarding was associated with a general rise in male stress hormone levels but, from a certain threshold of mate-guarding onwards, increased vigilance time was associated with a decrease in stress hormone output. Mate-guarding also increased male-male aggression rate and male vigilance time. Overall, alpha males were more physiologically stressed than other males independently of mating competition. Increased glucocorticoid levels during mate-guarding are most likely adaptive since it may help males to mobilize extra-energy required for mate-guarding and ultimately maintain a balanced energetic status. However, repeated exposure to high levels of stress over an extended period is potentially deleterious to the immune system and thus may carry costs. This potential physiological cost together with the cost of increased aggression mate-guarding male face may limit the males ability to mate-guard females, explaining the deviance from the PoA model observed in long-tailed macaques. Comparing our results to previous findings we discuss how ecological factors, reproductive seasonality and rank achievement may modulate the extent to which costs of mate-guarding limit male monopolization abilities.

Social and ecological factors influencing offspring survival in wild macaques

Lay summary Better to live in a big group if you want your offspring to survive! Using a multivariate approach, we show how the interplay of ecological and social factors influences fetus and infant survival in wild crested macaques. Offspring are more likely to survive in bigger groups, but seasonality also influences their survival. Fetus survival is higher for higher ranking mothers, whereas the main determinant of infants’ death is an alpha-male takeover by an immigrant male.

Alpha male replacements and delayed dispersal in crested macaques (Macaca nigra)

In species with a high male reproductive skew, competition between males for the top dominant position is high and escalated fights are common between competitors. As a consequence, challenges incur potentially high costs. Selection should favor males who time an alpha male challenge to maximize chances of a successful outcome minimizing costs. Despite the importance of alpha male replacements for individual males, we know little about the timing of challenges and the condition of the challenger. We investigated the timing and process of alpha male replacements in a species living in multi‐male groups with high male reproductive skew, the crested macaque. We studied four wild groups over 6 years in the Tangkoko Reserve, North Sulawesi, Indonesia, during which 16 alpha male replacements occurred. Although unusual for cercopithecines, male crested macaques delayed their natal dispersal until they attained maximum body mass and therefore fighting ability whereupon they emigrated and challenged the alpha male in another group. Accordingly, all observed alpha male replacements were from outside males. Ours is the first report of such a pattern in a primate species living in multi‐male groups. Although the majority of alpha male replacements occurred through direct male‐male challenges, many also took place opportunistically (i.e., after the alpha male had already been injured or had left the group). Furthermore, alpha male tenures were very short (averaging ca. 12 months). We hypothesize that this unusual pattern of alpha male replacements in crested macaques is related to the species‐specific combination of high male reproductive skew with a large number of males per group. Am. J. Primatol. 79:e22448, 2017.

Androgen correlates of male reproductive effort in wild male long-tailed macaques (Macaca fascicularis): A multi-level test of the challenge hypothesis

The challenge hypothesis (Wingfield et al., 1990) has been broadly utilised as a conceptual framework to study male androgen correlates of reproductive challenges in mammals. These studies mainly assessed male androgen responsiveness to a general degree of challenge over extended periods of time. Short term co-variation between the socio-sexual challenging context and androgen levels remains, however, largely understudied. We thus aim at providing a multi-level test of the challenge hypothesis by investigating the inter- and intra-individual variations in faecal androgen excretion associated to 1) breeding seasonality, 2) dominance rank, 3) mate-guarding activity and 4) value of the guarded female. We studied long-tailed macaques, a species in which males engage in highly challenging monopolisation of females over discreet periods of time. This particularity allows testing specifically the predicted increase from level B to level C in the challenge hypothesis. The study was carried out during two reproductive seasons on three groups of wild long-tailed macaques. We combined behavioural observations and non-invasive measurements of faecal androgen metabolite (fAM) levels. We found that, as predicted by the challenge hypothesis, male long-tailed macaques respond not only to seasonal but also to short term reproductive challenges by adapting their androgen levels. First, males exhibited a seasonal rise in fAM levels during the mating period which may be triggered by fruit availability as shown by our phenological data. Second, males had increased androgen levels when mate-guarding females and, across mate-guarding periods, males had higher fAM levels when monopolising high-ranking parous females than when monopolising low-ranking ones. Finally, high-ranking males had higher fAM levels than low-ranking males year round. Our study confirms that, in species with a high degree of female monopolisability, androgen may be an important physiological fitness enhancing tool for males by increasing female monopolisation efficiency (in particular with highly valuable females) and helping males to respond to rank take-over challenges.

Costs of and Investment in Mate-Guarding in Wild Long-Tailed Macaques (Macaca fascicularis): Influences of Female Characteristics and Male-Female Social Bonds

Male primates living in multimale groups tend to direct mate and mate-guarding choices toward females of high reproductive value, i.e., high-ranking, parous females, or females with which they share strong bonds. Little is known, however, about the constraints that may limit male mate-guarding choices (the costs of this behavior) and the influence of the females’ quality on male investment in mate-guarding. We aimed to study the effects of female rank, parity status, and male–female social bond strength on the costs of and investment in mate-guarding by males. We carried out our study during two reproductive seasons on three groups of wild long-tailed macaques in Indonesia. We combined behavioral observations on male locomotion and activity with noninvasive measurements of fecal glucocorticoids (fGC). Males spent less time feeding when mate-guarding nulliparous females than when mate-guarding parous females and tended to have higher fGC levels when mate-guarding low-ranking nulliparous females than when mate-guarding high-ranking nulliparous ones. Evolution should thus favor male choice for high-ranking parous females because such a decision brings benefits at proximate (reduced costs of mate-guarding) and ultimate (higher reproductive value) levels. Further, male investment in mate-guarding was flexible and contingent on female reproductive and social value. Males were more vigilant and more aggressive toward other males when mate-guarding females to which they were strongly bonded and/or high-ranking ones than when mate-guarding other females. Our findings bring a new dimension to the study of mate choice by showing that males not only mate preferentially with high-quality females but may also aim to secure paternity with these females through optimized monopolization.