Morphological variability or inter-observer bias? A methodological toolkit to improve data quality of multi-researcher datasets for the analysis of morphological variation.

OBJECTIVES: The investigation of morphological variation in animals is widely used in taxonomy, ecology, and evolution. Using large datasets for meta-analyses has dramatically increased, raising concerns about dataset compatibilities and biases introduced by contributions of multiple researchers. MATERIALS AND METHODS: We compiled morphological data on 13 variables for 3073 individual mouse lemurs (Cheirogaleidae, Microcebus spp.) from 25 taxa and 153 different sampling locations, measured by 48 different researchers. We introduced and applied a filtering pipeline and quantified improvements in data quality (Shapiro-Francia statistic, skewness, and excess kurtosis). The filtered dataset was then used to test for genus-wide sexual size dimorphism and the applicability of Rensch's, Allen's, and Bergmann's rules. RESULTS: Our pipeline reduced inter-observer bias (i.e., increased normality of data distributions). Inter-observer reliability of measurements was notably variable, highlighting the need to reduce data collection biases. Although subtle, we found a consistent pattern of sexual size dimorphism across Microcebus, with females being the larger (but not heavier) sex. Sexual size dimorphism was isometric, providing no support for Rensch's rule. Variations in tail length but not in ear size were consistent with the predictions of Allen's rule. Body mass and length followed a pattern contrary to predictions of Bergmann's rule. DISCUSSION: We highlighted the usefulness of large multi-researcher datasets for testing ecological hypotheses after correcting for inter-observer biases. Using genus-wide tests, we outlined generalizable patterns of morphological variability across all mouse lemurs. This new methodological toolkit aims to facilitate future large-scale morphological comparisons for a wide range of taxa and applications.

Stillbirth of a mandrill (Mandrillus sphinx) in the wild: perinatal behaviors and delivery sequences.

Birth is a fundamental event in the life of animals, including our own species. More reports of wild non-human primate births and stillbirths are thus needed to better understand the evolutionary pressures shaping parturition behaviors in our lineage. In diurnal non-human primates, births generally occur at night, when individuals are resting. Consequently, they are difficult to observe in the wild and most of the current knowledge regarding perinatal behaviors comes from rare daytime births. Information about stillbirths is even rarer and their proximate causes are generally unknown. Here, we present detailed observations of a daytime birth of a stillborn wild mandrill (Mandrillus sphinx). During this event, which lasted an entire day, we recorded the behaviors of the parturient female ad libitum, using video recordings and photos. The 5-year-old female was primiparous and of low dominance rank. The length of her pregnancy was shorter than usual and the partum phase was extremely long compared to other birth reports in non-human primates. The female disappeared shortly after this event and was assumed to have died. We discuss the possible causes of this stillbirth including the infant's presentation at birth and maternal inexperience.

Cognitive performance is linked to fitness in a wild primate.

Cognitive performance varies widely across animal species, but the processes underlying cognitive evolution remain poorly known. For cognitive abilities to evolve, performance must be linked to individual fitness benefits, but these links have been rarely studied in primates even though they exceed most other mammals in these traits. We subjected 198 wild gray mouse lemurs to four cognitive and two personality tests and subsequently monitored their survival in a mark-recapture study. Our study revealed that survival was predicted by individual variation in cognitive performance as well as body mass and exploration. Because cognitive performance covaried negatively with exploration, individuals gathering more accurate information enjoyed better cognitive performance and lived longer, but so did heavier and more explorative individuals. These effects may reflect a speed-accuracy trade-off, with alternative strategies yielding similar overall fitness. The observed intraspecific variation in selective benefits of cognitive performance, if heritable, can provide the basis for the evolution of cognitive abilities in members of our lineage.

Destabilizing effect of climate change on the persistence of a short-lived primate.

Seasonal tropical environments are among those regions that are the most affected by shifts in temperature and rainfall regimes under climate change, with potentially severe consequences for wildlife population persistence. This persistence is ultimately determined by complex demographic responses to multiple climatic drivers, yet these complexities have been little explored in tropical mammals. We use long-term, individual-based demographic data (1994 to 2020) from a short-lived primate in western Madagascar, the gray mouse lemur (Microcebus murinus), to investigate the demographic drivers of population persistence under observed shifts in seasonal temperature and rainfall. While rainfall during the wet season has been declining over the years, dry season temperatures have been increasing, with these trends projected to continue. These environmental changes resulted in lower survival and higher recruitment rates over time for gray mouse lemurs. Although the contrasting changes have prevented the study population from collapsing, the resulting increase in life-history speed has destabilized an otherwise stable population. Population projections under more recent rainfall and temperature levels predict an increase in population fluctuations and a corresponding increase in the extinction risk over the next five decades. Our analyses show that a relatively short-lived mammal with high reproductive output, representing a life history that is expected to closely track changes in its environment, can nonetheless be threatened by climate change.

Biological sex is binary, even though there is a rainbow of sex roles: Denying biological sex is anthropocentric and promotes species chauvinism: Denying biological sex is anthropocentric and promotes species chauvinism.

Biomedical and social scientists are increasingly calling the biological sex into question, arguing that sex is a graded spectrum rather than a binary trait. Leading science journals have been adopting this relativist view, thereby opposing fundamental biological facts. While we fully endorse efforts to create a more inclusive environment for gender-diverse people, this does not require denying biological sex. On the contrary, the rejection of biological sex seems to be based on a lack of knowledge about evolution and it champions species chauvinism, inasmuch as it imposes human identity notions on millions of other species. We argue that the biological definition of the sexes remains central to recognising the diversity of life. Humans with their unique combination of biological sex and gender are different from non-human animals and plants in this respect. Denying the concept of biological sex, for whatever cause, ultimately erodes scientific progress and may open the flood gates to "alternative truths."

Sex roles and sex ratios in animals.

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.

Adult sex ratios: causes of variation and implications for animal and human societies.

Converging lines of inquiry from across the social and biological sciences target the adult sex ratio (ASR; the proportion of males in the adult population) as a fundamental population-level determinant of behavior. The ASR, which indicates the relative number of potential mates to competitors in a population, frames the selective arena for competition, mate choice, and social interactions. Here we review a growing literature, focusing on methodological developments that sharpen knowledge of the demographic variables underlying ASR variation, experiments that enhance understanding of the consequences of ASR imbalance across societies, and phylogenetic analyses that provide novel insights into social evolution. We additionally highlight areas where research advances are expected to make accelerating contributions across the social sciences, evolutionary biology, and biodiversity conservation.

Mandrill mothers associate with infants who look like their own offspring using phenotype matching.

Behavioral discrimination of kin is a key process structuring social relationships in animals. In this study, we provide evidence for discrimination towards non-kin by third-parties through a mechanism of phenotype matching. In mandrills, we recently demonstrated increased facial resemblance among paternally related juvenile and adult females indicating adaptive opportunities for paternal kin recognition. Here, we hypothesize that mandrill mothers use offspring's facial resemblance with other infants to guide offspring's social opportunities towards similar-looking ones. Using deep learning for face recognition in 80 wild mandrill infants, we first show that infants sired by the same father resemble each other the most, independently of their age, sex or maternal origin, extending previous results to the youngest age class. Using long-term behavioral observations on association patterns, and controlling for matrilineal origin, maternal relatedness and infant age and sex, we then show, as predicted, that mothers are spatially closer to infants that resemble their own offspring more, and that this maternal behavior leads to similar-looking infants being spatially associated. We then discuss the different scenarios explaining this result, arguing that an adaptive maternal behavior is a likely explanation. In support of this mechanism and using theoretical modeling, we finally describe a plausible evolutionary process whereby mothers gain fitness benefits by promoting nepotism among paternally related infants. This mechanism, that we call 'second-order kin selection', may extend beyond mother-infant interactions and has the potential to explain cooperative behaviors among non-kin in other social species, including humans.

Evaluating expert-based habitat suitability information of terrestrial mammals with GPS-tracking data.

Aim: Macroecological studies that require habitat suitability data for many species often derive this information from expert opinion. However, expert-based information is inherently subjective and thus prone to errors. The increasing availability of GPS tracking data offers opportunities to evaluate and supplement expert-based information with detailed empirical evidence. Here, we compared expert-based habitat suitability information from the International Union for Conservation of Nature (IUCN) with habitat suitability information derived from GPS-tracking data of 1,498 individuals from 49 mammal species. Location: Worldwide. Time period: 1998-2021. Major taxa studied: Forty-nine terrestrial mammal species. Methods: Using GPS data, we estimated two measures of habitat suitability for each individual animal: proportional habitat use (proportion of GPS locations within a habitat type), and selection ratio (habitat use relative to its availability). For each individual we then evaluated whether the GPS-based habitat suitability measures were in agreement with the IUCN data. To that end, we calculated the probability that the ranking of empirical habitat suitability measures was in agreement with IUCN's classification into suitable, marginal and unsuitable habitat types. Results: IUCN habitat suitability data were in accordance with the GPS data (> 95% probability of agreement) for 33 out of 49 species based on proportional habitat use estimates and for 25 out of 49 species based on selection ratios. In addition, 37 and 34 species had a > 50% probability of agreement based on proportional habitat use and selection ratios, respectively. Main conclusions: We show how GPS-tracking data can be used to evaluate IUCN habitat suitability data. Our findings indicate that for the majority of species included in this study, it is appropriate to use IUCN habitat suitability data in macroecological studies. Furthermore, we show that GPS-tracking data can be used to identify and prioritize species and habitat types for re-evaluation of IUCN habitat suitability data.

Coevolution of social and communicative complexity in lemurs.

The endemic lemurs of Madagascar (Lemuriformes: Primates) exhibit great social and communicative diversity. Given their independent evolutionary history, lemurs provide an excellent opportunity to identify fundamental principles in the coevolution of social and communicative traits. We conducted comparative phylogenetic analyses to examine patterns of interspecific variation among measures of social complexity and repertoire sizes in the vocal, olfactory and visual modality, while controlling for environmental factors such as habitat and number of sympatric species. We also examined potential trade-offs in signal evolution as well as coevolution between body mass or brain size and communicative complexity. Repertoire sizes in the vocal, olfactory and visual modality correlated positively with group size, but not with environmental factors. Evolutionary changes in social complexity presumably antedated corresponding changes in communicative complexity. There was no trade-off in the evolution of signals in different modalities and neither body mass nor brain size correlated with any repertoire size. Hence, communicative complexity coevolved with social complexity across different modalities, possibly to service social relationships flexibly and effectively in pair- and group-living species. Our analyses shed light on the requirements and adaptive possibilities in the coevolution of core elements of social organization and social structure in a basal primate lineage. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Sex-specific movement ecology of the shortest-lived tetrapod during the mating season.

Sex-specific reproductive strategies are shaped by the distribution of potential mates in space and time. Labord's chameleon (Furcifer labordi) from southwestern Madagascar is the shortest-lived tetrapod whose life-time mating opportunities are restricted to a few weeks. Given that these chameleons grow to sexual maturity within about three months and that all individuals die soon after breeding, their mating strategies should be adapted to these temporal constraints. The reproductive tactics of this or any other Malagasy chameleon species have not been studied, however. Radio-tracking and observations of 21 females and 18 males revealed that females exhibit high site fidelity, move small cumulative and linear distances, have low corresponding dispersal ratios and small occurrence distributions. In contrast, males moved larger distances in less predictable fashion, resulting in dispersal ratios and occurrence distributions 7-14 times larger than those of females, and males also had greater ranges of their vertical distribution. Despite synchronous hatching, males exhibited substantial inter-individual variation in body mass and snout-vent length that was significantly greater than in females, but apparently unrelated to their spatial tactics. Females mated with up to 6 individually-known mates, but frequent encounters with unmarked individuals indicate that much higher number of matings may be common, as are damaging fights among males. Thus, unlike perennial chameleons, F. labordi males do not seem to maintain and defend territories. Instead, they invest vastly more time and energy into locomotion for their body size than other species. Pronounced variation in key somatic traits may hint at the existence of alternative reproductive tactics, but its causes and consequences require further study. This first preliminary study of the mating system of a Malagasy chameleon indicates that, as in other semelparous tetrapods, accelerated life histories are tied to a mating system with intense contest and scramble competition among males.

The eco-evolutionary landscape of power relationships between males and females.

In animal societies, control over resources and reproduction is often biased towards one sex. Yet, the ecological and evolutionary underpinnings of male-female power asymmetries remain poorly understood. We outline a comprehensive framework to quantify and predict the dynamics of male-female power relationships within and across mammalian species. We show that male-female power relationships are more nuanced and flexible than previously acknowledged. We then propose that enhanced reproductive control over when and with whom to mate predicts social empowerment across ecological and evolutionary contexts. The framework explains distinct pathways to sex-biased power: coercion and male-biased dimorphism constitute a co-evolutionary highway to male power, whereas female power emerges through multiple physiological, morphological, behavioural, and socioecological pathways.

Sex bias in intergroup conflict and collective movements among social mammals: male warriors and female guides.

Intergroup conflict is a major evolutionary force shaping animal and human societies. Males and females should, on average, experience different costs and benefits for participating in collective action. Specifically, among mammals, male fitness is generally limited by access to mates whereas females are limited by access to food and safety. Here we analyse sex biases among 72 species of group-living mammals in two contexts: intergroup conflict and collective movements. Our comparative phylogenetic analyses show that the modal mammalian pattern is male-biased participation in intergroup conflict and female-biased leadership in collective movements. However, the probability of male-biased participation in intergroup conflicts decreased and female-biased participation increased with female-biased leadership in movements. Thus, female-biased participation in intergroup conflict only emerged in species with female-biased leadership in collective movements, such as in spotted hyenas and some lemurs. Sex differences are probably attributable to costs and benefits of participating in collective movements (e.g. towards food, water, safety) and intergroup conflict (e.g. access to mates or resources, risk of injury). Our comparative review offers new insights into the factors shaping sex bias in leadership across social mammals and is consistent with the 'male warrior hypothesis' which posits evolved sex differences in human intergroup psychology. This article is part of the theme issue 'Intergroup conflict across taxa'.

Sex differences in audience effects on anogenital scent marking in the red-fronted lemur.

How the presence of conspecifics affects scent mark deposition remains an understudied aspect of olfactory communication, even though scent marking occurs in different social contexts. Sex differences in scent-marking behaviour are common, and sex-specific effects of the audience could therefore be expected. We investigated sex differences in intra-group audience effects on anogenital scent marking in four groups of wild red-fronted lemurs (Eulemur rufifrons) by performing focal scent-marking observations. We observed a total of 327 events divided into 223 anogenital scent-marking events and 104 pass-by events (i.e. passage without scent marking). Using a combination of generalised linear mixed models and exponential random graph models, we found that scent marking in red-fronted lemurs is associated with some behavioural flexibility linked to the composition of the audience at the time of scent deposition. In particular, our study revealed sex differences in the audience effects, with males being overall more sensitive to their audience than females. Moreover, we show that these audience effects were dependent on the relative degree of social integration of the focal individual compared to that of individuals in the audience (difference in Composite Sociality Index) as well as the strength of the dyadic affiliative relationship (rank of Dyadic Composite Sociality Index within the group). The audience effects also varied as a function of the audience radius considered. Hence, we showed that scent marking in red-fronted lemurs is associated with some behavioural flexibility linked to the composition of the audience, ascribing red-fronted lemurs' social competence in this context.

Drivers of gut microbiome variation within and between groups of a wild Malagasy primate.

BACKGROUND: Various aspects of sociality can benefit individuals' health. The host social environment and its relative contributions to the host-microbiome relationship have emerged as key topics in microbial research. Yet, understanding the mechanisms that lead to structural variation in the social microbiome, the collective microbial metacommunity of an animal's social network, remains difficult since multiple processes operate simultaneously within and among animal social networks. Here, we examined the potential drivers of the convergence of the gut microbiome on multiple scales among and within seven neighbouring groups of wild Verreaux's sifakas (Propithecus verreauxi) - a folivorous primate of Madagascar. RESULTS: Over four field seasons, we collected 519 faecal samples of 41 animals and determined gut communities via 16S and 18S rRNA gene amplicon analyses. First, we examined whether group members share more similar gut microbiota and if diet, home range overlap, or habitat similarity drive between-group variation in gut communities, accounting for seasonality. Next, we examined within-group variation in gut microbiota by examining the potential effects of social contact rates, male rank, and maternal relatedness. To explore the host intrinsic effects on the gut community structure, we investigated age, sex, faecal glucocorticoid metabolites, and female reproductive state. We found that group members share more similar gut microbiota and differ in alpha diversity, while none of the environmental predictors explained the patterns of between-group variation. Maternal relatedness played an important role in within-group microbial homogeneity and may also explain why adult group members shared the least similar gut microbiota. Also, dominant males differed in their bacterial composition from their group mates, which might be driven by rank-related differences in physiology and scent-marking behaviours. Links to sex, female reproductive state, or faecal glucocorticoid metabolites were not detected. CONCLUSIONS: Environmental factors define the general set-up of population-specific gut microbiota, but intrinsic and social factors have a stronger impact on gut microbiome variation in this primate species. Video abstract.

Linking cognition to ecology in wild sympatric mouse lemur species.

Cognitive abilities covary with both social and ecological factors across animal taxa. Ecological generalists have been attributed with enhanced cognitive abilities, but which specific ecological factors may have shaped the evolution of which specific cognitive abilities remains poorly known. To explore these links, we applied a cognitive test battery (two personality, ten cognitive tests; n = 1104 tests) to wild individuals of two sympatric mouse lemur species (n = 120 Microcebus murinus, n = 34 M. berthae) varying in ecological adaptations but sharing key features of their social systems. The habitat and dietary generalist grey mouse lemurs were more innovative and exhibited better spatial learning abilities; a cognitive advantage in responding adaptively to dynamic environmental conditions. The more specialized Madame Berthe's mouse lemurs were faster in learning associative reward contingencies, providing relative advantages in stable environmental conditions. Hence, our study revealed key cognitive correlates of ecological adaptations and indicates potential cognitive constraints of specialists that may help explain why they face a greater extinction risk in the context of current environmental changes.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Life on the edge: behavioural and physiological responses of Verreaux's sifakas (Propithecus verreauxi) to forest edges.

Forest edges change micro-environmental conditions, thereby affecting the ecology of many forest-dwelling species. Understanding such edge effects is particularly important for Malagasy primates because many of them live in highly fragmented forests today. The aim of our study was to assess the influence of forest edge effects on activity budgets, feeding ecology, and stress hormone output (measured as faecal glucocorticoid metabolite - fGCM - levels) in wild Verreaux's sifakas (Propithecus verreauxi), a group living, arboreal lemur. We observed five habituated groups: three living in the forest interior and two at an established forest edge. There was no difference in average daily temperatures between edge and interior habitats; however, within the edge site, the average daily temperature incrementally increased over 450 m from the forest edge towards the interior forest of the edge habitat, and the population density was lower at the edge site. Activity budgets differed between groups living in the two microhabitats, with individuals living near the edge spending more time travelling and less time feeding. Groups living near the edge also tended to have smaller home ranges and core areas than groups in the forest interior. In addition, edge groups had elevated average fGCM concentrations, and birth rates were lower for females living in the edge habitat. Combined with lower levels of fruit consumption at the edge, these results suggest that nutritional stress might be a limiting factor for Verreaux's sifakas when living near a forest edge. Hence, Verreaux's sifakas appear to be sensitive to microhabitat characteristics linked to forest edges; a result with implications for the conservation of this critically endangered lemurid species.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.