Assortative mating by size: A meta-analysis of mating patterns in water striders

Summary Assortative mating by size is a common mating pattern that can be generated by several different behavioural mechanisms, with different evolutionary implications. Assortative mating is typically associated with sexual selection and has been regarded as an attribute of populations, species, mating systems or even higher order taxa. In most animal groups, however, appropriate analyses of assortative mating at these different levels are lacking and the causes and forms of assortative mating are poorly understood. Here, we analyse 45 different population level estimates of assortative mating and non-random mating by size in seven confamiliar species of water striders that share a common mating system. A hierarchical comparative analysis shows that virtually all the variance within the clade occurs among samples within species. We then employ meta-analysis to estimate the overall strength of assortative mating, to determine the form of assortative mating and to further assess potential differences among species as well as the probable causes of assortative mating in this group of insects. We found overall weak but highly significant positive assortative mating. We show that analyses of the degree of heteroscedasticity in plots of male versus female size are critical, since the evolutionary implications of true and apparent assortative mating differ widely and conclude that the positive assortative mating observed in water striders was of the true rather than the apparent form. Further, within samples, mating individuals were significantly larger than non-mating individuals in both males and females. All of these non-random mating patterns were consistent among species and we conclude that weak positive assortative mating by size is a general characteristic of those water strider species that share this mating system. We use our results to illustrate the importance of distinguishing between different forms of assortative mating, to discriminate between various behavioural causes of assortative mating and to assess potential sources of interpopulational variance in estimates of assortative mating. Finally, we discuss the value of using meta-analytic techniques for detecting overall patterns in multiple studies of non-random mating.     

The scale‐of‐choice effect and how estimates of assortative mating in the wild can be biased due to heterogeneous samples

The mode in which sexual organisms choose mates is a key evolutionary process, as it can have a profound impact on fitness and speciation. One way to study mate choice in the wild is by measuring trait correlation between mates. Positive assortative mating is inferred when individuals of a mating pair display traits that are more similar than those expected under random mating while negative assortative mating is the opposite. A recent review of 1134 trait correlations found that positive estimates of assortative mating were more frequent and larger in magnitude than negative estimates. Here, we describe the scale‐of‐choice effect (SCE), which occurs when mate choice exists at a smaller scale than that of the investigator's sampling, while simultaneously the trait is heterogeneously distributed at the true scale‐of‐choice. We demonstrate the SCE by Monte Carlo simulations and estimate it in two organisms showing positive (Littorina saxatilis) and negative (L. fabalis) assortative mating. Our results show that both positive and negative estimates are biased by the SCE by different magnitudes, typically toward positive values. Therefore, the low frequency of negative assortative mating observed in the literature may be due to the SCE's impact on correlation estimates, which demands new experimental evaluation.     

Sampling scale can cause bias in positive assortative mating estimates: evidence from two intertidal snails

Assortative mating in the wild is commonly estimated by correlating between traits in mating pairs (e.g. the size of males and females). Unfortunately, such an approach may suffer from considerable sampling bias when the distribution of different expressions of a trait in the wild is nonrandom (e.g. when segregation of different size classes of individuals occurs in different microhabitats or areas). Consequently, any observed trait correlation in the wild can be an artefact of pooling heterogeneous samples of mating pairs from different microhabitats or areas rather than true nonrandom matings. This bias in estimating trait correlations as a result of sampling scale is termed the scale‐of‐choice effect (SCE). In the present study, we use two intertidal littorinid species from Hong Kong to show how the SCE can bias size‐assortative mating estimates from mating pairs captured in the wild, empirically demonstrating the influence of this effect on measures of positive assortative mating. This finding cautions that studies overlooking the SCE may have misinterpreted the magnitude and the cause of assortative mating, and we provide a new analytical approach for protecting against this potential bias in future studies.     

Nuclear markers,mitochondrial DNA and male secondary sexual traits variation in a newt hybrid zone (Triturus vulgaris x T. montandoni)

The smooth and the Montandon's newts (Triturus vulgaris and T. montandoni) are genetically similar sister species with highly divergent male secondary sexual traits involved in complex courtship behaviour. Their parapatric ranges overlap at moderate elevations in the Carpathian Mountains where they hybridize readily. Here we present a detailed study of genetic and morphological variation in populations from the area of sympatry. Analysis of variation at seven nuclear markers, mtDNA and male sexual secondary traits was complemented with an ecological survey of breeding sites characteristics. Extensive hybridization was revealed with back-cross individuals similar to either parental species predominating among hybrids. The hybrid zone exhibited a mosaic pattern: the genetic composition of the populations was correlated only weakly with their geographical position. No association with habitat type was found. Departures from Hardy-Weinberg proportions, significant linkage disequilibria and bimodal distribution of genotypes suggest strongly that assortative mating is an important factor shaping the genetic composition of hybrid populations. The pattern of cytonuclear disequilibria did not indicate much asymmetry in interspecific matings. Changes in the frequency of nuclear markers were highly concordant, whereas mtDNA showed much wider bidirectional introgression with 14% excess of T. montandoni haplotype. We argue that the mosaic structure of the newt hybrid zone results mainly from stochastic processes related to extinction and recolonization. Microgeographical differences in mtDNA introgression are explained by historical range shifts. Since morphologically intermediate males were underrepresented when compared to hybrid males identified by genetic markers, sexual selection acting against the morphological intermediates is implied. We discuss the implications of these findings in the context of reinforcement of prezygotic isolation in newts.     

A novel method for estimating the strength of positive mating preference by similarity in the wild

Mating preference can be a driver of sexual selection and assortative mating and is, therefore, a key element in evolutionary dynamics. Positive mating preference by similarity is the tendency for the choosy individual to select a mate which possesses a similar variant of a trait. Such preference can be modelled using Gaussian‐like mathematical functions that describe the strength of preference, but such functions cannot be applied to empirical data collected from the field. As a result, traditionally, mating preference is indirectly estimated by the degree of assortative mating (using Pearson's correlation coefficient, r) in wild captured mating pairs. Unfortunately, r and similar coefficients are often biased due to the fact that different variants of a given trait are nonrandomly distributed in the wild, and pooling of mating pairs from such heterogeneous samples may lead to “false–positive” results, termed “the scale‐of‐choice effect” (SCE). Here we provide two new estimators of mating preference (C_rough and C_scaled) derived from Gaussian‐like functions which can be applied to empirical data. Computer simulations demonstrated that r coefficient showed robust estimations properties of mating preference but it was severely affected by SCE, C_rough showed reasonable estimation properties and it was little affected by SCE, while C_scaled showed the best properties at infinite sample sizes and it was not affected by SCE but failed at biological sample sizes. We recommend using C_rough combined with the r coefficient to infer mating preference in future empirical studies.     

A comparative study of Gaussian mating preference functions: a key element of sympatric speciation models

Simulating the evolution of reproductive isolation under sympatric speciation scenarios is a complex process that requires modelling several phases, including evolution of phenotypes, demography, migration, fitness components and mating preference. The last has been shown to be a key parameter in several simulation studies, allowing the incorporation of assortative mating (premating isolation). Mating preference can be modelled by different mathematical functions but, as far as we know, a formal comparison of those functions has not yet been undertaken. In this work, we briefly review the main functions used in the literature and suggest a new one. In doing so, we also define three basic properties (monotonicity, proportionality and symmetry) that an ideal function should satisfy when generating assortative mating. We simulated several scenarios to compare how all these functions perform based on these properties. We also draw attention to the fact that the existing functions are affected distinctly by changing the scale of the preferred trait value. Some functions remain unaffected by scaling the trait, while in others assortative mating increases proportionally to the trait value. Most of the functions tested did not fulfil all the properties studied, and we find certain flaws in some of them that should be considered before being used in future studies. We provide some general recommendations for using the preference functions in simulation studies, and suggest that an unnoticed scaling effect could have underestimated the chance to obtain speciation under certain scenarios. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 642–657.     

Assortative mating in two populations of Short‐tailed Albatross Phoebastria albatrus on Torishima

Assortative mating is an important pre‐mating isolation mechanism that has been observed in some wild populations of seabirds. The Short‐tailed Albatross Phoebastria albatrus is a globally Vulnerable seabird that breeds mainly on Torishima and the Senkaku Islands in the north‐western Pacific Ocean. Our previous studies suggested that two genetically distinct populations exist, one on Torishima and the other on the Senkaku Islands. Recently, however, several un‐ringed birds in subadult plumage have been observed breeding on Torishima in the Hatsunezaki colony. As almost all birds hatched on Torishima since 1979 have been ringed, the natal site of the un‐ringed birds was suspected to be the Senkaku Islands. Genetic differences between the two populations would reveal the natal sites of un‐ringed birds. By observing the ring status (ringed or un‐ringed) of mating pairs and analysing the mitochondrial DNA (mtDNA) control region 2 of un‐ringed birds, we assessed whether birds that originated from Torishima and the Senkaku Islands achieved pre‐mating isolation. There was a small number of pairs on Torishima that consisted of one ringed and one un‐ringed bird, but the observed number was significantly lower than that expected if ringed and un‐ringed birds mated randomly. Furthermore, mtDNA analyses of nine un‐ringed birds demonstrated that all belonged to a particular haplotype clade from the Senkaku Islands. These results show that birds from Torishima and the Senkaku Islands mate assortatively but that there is incomplete pre‐mating isolation between birds from the two island groups. The pre‐mating isolation of these two populations of Short‐tailed Albatross could arise from differences in the timing of breeding and incompatibility in mating displays. As the divergence between the two populations is unlikely to be sufficient to achieve complete post‐mating isolation, the two groups are likely to be hybridizing. Further studies using molecular and/or behavioural analyses would be required to reveal the evolutionary significance of hybridization between these two populations.     

Conditions for sympatric speciation: A diploid model incorporating habitat fidelity and non-habitat assortative mating

Summary Three types of genes have been proposed to promote sympatric speciation: habitat preference genes, assortative mating genes and habitat-based fitness genes. Previous computer models have analysed these genes separately or in pairs. In this paper we describe a multilocus model in which genes of all three types are considered simultaneously. Our computer simulations show that speciation occurs in complete sympatry under a broad range of conditions. The process includes an initial diversification phase during which a slight amount of divergence occurs, a quasi-equilibrium phase of stasis during which little or no detectable divergence occurs and a completion phase during which divergence is dramatic and gene flow between diverging habitat morphs is rapidly eliminated. Habitat preference genes and habitat-specific fitness genes become associated when assortative mating occurs due to habitat preference, but interbreeding between individuals adapted to different habitats occurs unless habitat preference is almost error free. However, nonhabitat assortative mating, when coupled with habitat preference can eliminate this interbreeding. Even when several loci contribute to the probability of expression of non-habitat assortative mating and the contributions of individual loci are small, gene flow between diverging portions of the population can terminate within less than 1000 generations.     

Emergence and loss of assortative mating in sympatric speciation

We have studied an agent model which presents the emergence of sexual barriers through the onset of assortative mating, a condition that might lead to sympatric speciation. In the model, individuals are characterized by two traits, each determined by a single locus A or B. Heterozygotes on A are penalized by introducing an adaptive difference from homozygotes. Two niches are available. Each A homozygote is adapted to one of the niches. The second trait, called the marker trait has no bearing on the fitness. The model includes mating preferences, which are inherited from the mother and subject to random variations. A parameter controlling recombination probabilities of the two loci is also introduced. We study the phase diagram by means of simulations, in the space of parameters (adaptive difference, carrying capacity, recombination probability). Three phases are found, characterized by (i) assortative mating, (ii) extinction of one of the A alleles and (iii) Hardy-Weinberg like equilibrium. We also make perturbations of these phases to see how robust they are. Assortative mating can be gained or lost with changes that present hysteresis loops, showing the resulting equilibrium to have partial memory of the initial state and that the process of going from a polymorphic panmictic phase to a phase where assortative mating acts as sexual barrier can be described as a first-order transition.     

Emergence and Maintenance of Sex among Diploid Organisms Aided by Assortative Mating

Using computer simulations I studied the simultaneous effect of variable environments, mutation rates, ploidy, number of loci subject to evolution and random and assortative mating on various reproductive systems. The simulations showed that mutants for sex and recombination are evolutionarily stable, displacing alleles for monosexuality in diploid populations mating assortatively under variable selection pressure. Assortative mating reduced excessive allelic variance induced by recombination and sex, especially among diploids. Results suggest a novel adaptive value for sex and recombination. They show that the adaptive value of diploidy and that of the segregation of sexes is different to that of sex and recombination. The results suggest that the emergence of sex had to be preceded by the emergence of diploid monosexual organisms and provide an explanation for the emergence and maintenance of sex among diploids and for the scarcity of sex among haploid organisms.     

An analysis of genetic differentiation among assortatively mating Drosophila melanogaster in Zimbabwe

African Drosophila melanogaster populations, and those from Zimbabwe in particular, have attracted much interest recently. African flies differ genetically from 'cosmopolitan' populations and were found to exhibit discriminative mating behaviour against individuals from 'cosmopolitan' populations. It has therefore been proposed that Zimbabwean and some other African populations are in an 'incipient stage of speciation'. However, whether the mating behaviour is an effective barrier against gene flow from other populations, and whether intra-population genetic differentiation has already evolved in sympatry is not known. Here, we took a population-based approach to test whether the well-characterized mating type differences have resulted in a genome-wide differentiation at the population level. Using 122 polymorphic microsatellite loci mapping to the third chromosome, we demonstrate a significant genetic differentiation between Zimbabwean flies differing in their mating behaviour. We also provide evidence to suggest that this difference is unlikely to be attributable to population structure within Zimbabwe. However, the analysis of individual microsatellite loci did not indicate more loci differentiating these two groups than expected by chance. Our data suggest that the 'Z'-'M' mating behaviour is strong enough to result in a small but significant genetic differentiation. Thus, future studies based on a larger population sample of flies characterized for their mating behaviour and using more markers are expected to provide more information on the genetic basis of the mating traits in the Zimbabwe flies.     

Assortative mating between two distinct micro-allopatric populations of Littorina saxatilis (Olivi) on the northeast coast of England

Size assortative mating is a common invertebrate mating pattern and is usually accompanied by male and female sexual selection, and these three behaviours can contribute to reproductive isolation. Two distinct populations of the marine prosobranch Littorina saxatilis, H and M, occur within 15 m of each other on the same shore. Previous studies have demonstrated that these two forms have different reproductive strategies and that the rare hybrids between the two forms show evidence of reproductive dysfunction and hence are less fit than the assumed parental forms. In both populations, female shell height was shown to be a predictor of the number of embryos contained within the brood pouch. The mean shell height of the M population was significantly larger than that of the H population, and the M population matures at a larger shell size than the H population. The two populations show complete assortative mating to type in the field, and occupy different microhabitats on the same shore. Therefore, laboratory-based experiments were performed to determine if assortative mating was maintained in sympatry and also to determine the effect of population density on mate choice. The males of both populations showed sexual selection for female size, choosing to mate with females approximately 10% larger than themselves from an assortment of female sizes. The M population showed complete assortative mating to type, irrespective of the density of H and M females, whereas at low densities the H males did occasionally mate with M females. The role of assortative mating and reinforcement (due to natural selection acting against the less fit hybrids), in maintaining the partial reproductive barrier between the two populations is discussed.     

Mechanisms of reinforcement in natural and simulated polymorphic populations

Reinforcement speciation is the process whereby selection against hybrids drives the evolution of enhanced pre‐mating reproductive isolation. Work has focused on divergent mating preferences (assortative mating) but pre‐mating isolation can also arise via various migration modification behaviours, such as divergent habitat preferences. The relative importance of these two different mechanisms of reinforcement remains unclear. A recent theoretical model (Yukilevich–True model) found that relative fixation probabilities between these mechanisms can vary. Additionally, natural populations of Timema cristinae walking‐sticks exhibit variation (polymorphism) in both mechanisms, generating questions about the patterns expected for allele frequencies prior to fixation, during the early stages of the speciation process. In the present study, we report: (1) new analyses examining the correlation between fixation probabilities for assortative mating and migration modification in the Yukilevich–True model; (2) novel simulations examining allele frequencies in polymorphic populations; and (3) empirical patterns of reinforcement in T. cristinae in the context of theoretical predictions. Simulations of both types yielded congruent results, revealing that the outcome of reinforcement was dependent on the strength of selection. Under weak selection, reinforcement by either mechanism is unlikely. Under intermediate selection, the conditions favoring the rise and fixation of one mechanism favored the rise and fixation of the other. However, assortative mating evolved somewhat more readily than migration modification. Populations of T. cristinae, which experience such intermediate selection, supported these predictions. Under strong selection, the evolution of migration modification generally interfered with the evolution of assortative mating by decreasing migration between populations, thereby reducing selection for assortative mating. Congruence of the results for allele frequencies versus fixation probabilities suggests that similar patterns of reinforcement are expected during different stages of the speciation process. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 305–319.     

Precopulatory mate assessment in relation to body size in the earthworm Lumbricus terrestris: avoidance of dangerous liaisons?

In the earthworm Lumbricus terrestris L., mating occurs on the soil surface, but partners remain anchored in their burrow andmating is preceded by repeated mutual burrow visits betweenneighbors. This study focuses on body size as one possibletrait that earthworms may assess during these burrow visits.Size-related mate choice is predicted to result in size-assortativemating, which we found in one field sample (n = 90 pairs),but not in a second (n = 102). We discovered that when mates separate, one of them can be pulled out of its burrow. Thiswas more likely for small individuals or those mating acrosswide distances. In a subsequent greenhouse experiment, we allowedfocal individuals to mate with two neighbors of different sizes.Relative size affected neither mating rate nor primary preference,but focals mated sooner with the same-sized neighbor than witha differently sized one. Small focals visited large neighborsmore often than small ones. We conclude that size influencesmate choice as well as the outcome of mating and discuss howthe "tug-of-war" that ends a mating contributes to this result.Precopulatory visits may involve assessment as well as enticementto lure the partner closer to the individual's own burrow,in order to minimize the risk when mating with a partner thatis large or far away.     

‘Prudent habitat choice’: a novel mechanism of size‐assortative mating

Assortative mating, an ubiquitous form of nonrandom mating, strongly impacts Darwinian fitness and can drive biological diversification. Despite its ecological and evolutionary importance, the behavioural processes underlying assortative mating are often unknown, and in particular, mechanisms not involving mate choice have been largely ignored so far. Here, we propose that assortative mating can arise from ‘prudent habitat choice’, a general mechanism that acts under natural selection, and that it can occur despite a complete mixing of phenotypes. We show that in the cichlid Eretmodus cyanostictus size‐assortative mating ensues, because individuals of weaker competitive ability ignore high‐quality but strongly competed habitat patches. Previous studies showed that in E. cyanostictus, size‐based mate preferences are absent. By field and laboratory experiments, here we showed that (i) habitat quality and body size are correlated in this species; (ii) territories with more stone cover are preferred by both sexes in the absence of competition; and (iii) smaller fish prudently occupy vacant territories of worse quality than do larger fish. Prudent habitat choice is likely to be a widespread mechanism of assortative mating, as both preferences for and dominance‐based access to high‐quality habitats are generic phenomena in animals.     

Heterozygosity-based assortative mating in blue tits (Cyanistes caeruleus): implications for the evolution of mate choice

The general hypothesis of mate choice based on non-additive genetic traits suggests that individuals would gain important benefits by choosing genetically dissimilar mates (compatible mate hypothesis) and/or more heterozygous mates (heterozygous mate hypothesis). In this study, we test these hypotheses in a socially monogamous bird, the blue tit (Cyanistes caeruleus). We found no evidence for a relatedness-based mating pattern, but heterozygosity was positively correlated between social mates, suggesting that blue tits may base their mating preferences on partner''s heterozygosity. We found evidence that the observed heterozygosity-based assortative mating could be maintained by both direct and indirect benefits. Heterozygosity reflected individual quality in both sexes: egg production and quality increased with female heterozygosity while more heterozygous males showed higher feeding rates during the brood-rearing period. Further, estimated offspring heterozygosity correlated with both paternal and maternal heterozygosity, suggesting that mating with heterozygous individuals can increase offspring genetic quality. Finally, plumage crown coloration was associated with male heterozygosity, and this could explain unanimous mate preferences for highly heterozygous and more ornamented individuals. Overall, this study suggests that non-additive genetic traits may play an important role in the evolution of mating preferences and offers empirical support to the resolution of the lek paradox from the perspective of the heterozygous mate hypothesis.     

The effect of positive assortative mating on genetic parameters in a simulated beef cattle population

Summary Two simulated data sets, representing random mating and positive assortative mating in a beef cattle population over 10 rounds of mating, were each composed of 100 replicates. Three correlated traits were considered; calving ease (CE), 200 day weight (WW) and postweaning gain (PG). All selection practiced in the simulation was random. Positive assortative mating, which was based on parental WW phenotypic records, increased the progeny additive genetic variance of WW. The absolute values of genetic covariances and correlations between WW with CE and PG were also increased by positive assortative mating. Variances or covariances did not reach their expected equilibrium values due to overlapping generations, low replacement rates and only 10 rounds of mating.The financial assistance of Agriculture Canada and the Natural Sciences and Engineering Research Council of Canada are gratefully acknowledged     

Directional selection on body size but no apparent survival cost to being large in wild New Zealand giraffe weevils

When an individual's reproductive success relies on winning fights to secure mating opportunities, bearing larger weapons is advantageous. However, sexual selection can be extremely complex, and over an animal's life the opportunity to mate is influenced by numerous factors. We studied a wild population of giraffe weevils (Lasiorhynchus barbicornis) that exhibit enormous intra and intersexual size variation. Males bear an elongated rostrum used as a weapon in fights for mating opportunities. However, small males also employ sneaking behavior as an alternative reproductive tactic. We investigated sexual selection on size by tracking individual males and females daily over two 30‐day periods to measure long‐term mating success. We also assessed how survival and recapture probabilities vary with sex and size to determine whether there might be a survival cost associated with size. We found evidence for directional selection on size through higher mating success, but no apparent survival trade‐off. Instead, larger individuals mate more often and have a higher survival probability, suggesting an accumulation of benefits to bigger individuals. Furthermore, we found evidence of size assortative mating where males appear to selectively mate with bigger females. Larger and more competitive males secure matings with larger females more frequently than smaller males, which may further increase their fitness.     

Courtship behavior,nesting microhabitat,and assortative mating in sympatric stickleback species pairs

The maintenance of reproductive isolation in the face of gene flow is a particularly contentious topic, but differences in reproductive behavior may provide the key to explaining this phenomenon. However, we do not yet fully understand how behavior contributes to maintaining species boundaries. How important are behavioral differences during reproduction? To what extent does assortative mating maintain reproductive isolation in recently diverged populations and how important are “magic traits”? Assortative mating can arise as a by‐product of accumulated differences between divergent populations as well as an adaptive response to contact between those populations, but this is often overlooked. Here we address these questions using recently described species pairs of three‐spined stickleback (Gasterosteus aculeatus), from two separate locations and a phenotypically intermediate allopatric population on the island of North Uist, Scottish Western Isles. We identified stark differences in the preferred nesting substrate and courtship behavior of species pair males. We showed that all males selectively court females of their own ecotype and all females prefer males of the same ecotype, regardless of whether they are from species pairs or allopatric populations. We also showed that mate choice does not appear to be driven by body size differences (a potential “magic trait”). By explicitly comparing the strength of these mating preferences between species pairs and single‐ecotype locations, we were able to show that present levels of assortative mating due to direct mate choice are likely a by‐product of other adaptations between ecotypes, and not subject to obvious selection in species pairs. Our results suggest that ecological divergence in mating characteristics, particularly nesting microhabitat may be more important than direct mate choice in maintaining reproductive isolation in stickleback species pairs.     

Close bonds and social rank similarities favor non-random mating in captive stump-tailed macaques (Macaca arctoides)

Assortative mating is non-random mating by the mutual choice of phenotypes or behavioral types. In polygynandrous species, competition for mating by social rank can lead to assortative mating. However, although not an individual trait, social bonds also influence mating opportunities resembling assortative mating. Stump-tailed macaques form long-term close bonds and organize in a linear dominance–subordination hierarchy. Therefore, we studied whether the strength of the social bond and rank closeness influenced mating decisions and increased mating opportunities, particularly for low- and middle-ranking animals. Firstly, we observed whether females directed proceptive behavior to close-bonded or adjacent rank males. Secondly, we measured whether successful copulations were related to the strength of social bonds and close ranking. Thirdly, to ensure that copulations owed mainly to the aforementioned factors, we also evaluated whether sexual coercion was unrelated to social bonds and rank similarities. Finally, we assessed whether close bonds mediated agonistic support to females. The study subjects were 12 adult female and 11 male captive stump-tailed macaques. We monitored daily females' reproductive status by vaginal cytology. Sexual behavior was recorded by all occurrences sampling and scan sampling to collect the agonistic and affiliative instances required to calculate social ranks, social bond strength, and agonistic support. The results indicated that the probability of females displaying proceptivity increased during the follicular phase toward close-bonded and high-ranking males. Copulation chances increased with male–female social bonds and rank closeness. Forced copulation decreased in close-bonded individuals, while agonistic support increased in close-ranking strong-bonded animals. In conclusion, close social bonds and similar social rank result in non-random mating in stump-tailed macaques.