Wayne L. Linklater

Social bonds between unrelated females increase reproductive success in feral horses

In many mammals, females form close social bonds with members of their group, usually between kin. Studies of social bonds and their fitness benefits have not been investigated outside primates, and are confounded by the relatedness between individuals in primate groups. Bonds may arise from kin selection and inclusive fitness rather than through direct benefits of association. However, female equids live in long-term social groups with unrelated members. We present 4 years of behavioral data, which demonstrate that social integration between unrelated females increases both foal birth rates and survival, independent of maternal habitat quality, social group type, dominance status, and age. Also, we show that such social integration reduces harassment by males. Consequently, social integration has strong direct fitness consequences between nonrelatives, suggesting that social bonds can evolve based on these direct benefits alone. Our results support recent studies highlighting the importance of direct benefits in maintaining cooperative behavior, while controlling for the confounding influence of kinship.

Stallion harassment and the mating system of horses

Feral horse, Equus caballus, breeding groups, called bands, usually include one but sometimes up to five stallions. We found that mares were loyal to single-stallion (SS) or multistallion (MS) bands or were social dispersers (maverick mares, Mv). The spacing and social behaviour of mares and stallions in single- and multistallion bands was measured. Indices of mare well-being were also measured including activity budgets (feeding: MS>SS=Mv; resting: MS<SS=Mv), band and mare travel (MS>SS), maternal effort in maintaining contact with foals (MS=Mv>SS), parasite levels in faeces (MS>Mv>SS), body condition (MS=Mv<SS), fecundity (Mv<MS<SS) and offspring mortality (Mv<MS<SS). We present evidence suggesting that the poorer well-being of maverick mares and multistallion band mares results from greater harassment by stallions. Stallion and mare behaviour and poor reproductive success in multistallion bands were not consistent with explanations for the existence of such bands based on cooperation or alternative mating strategies. We suggest an alternative explanation. Stable relationships between mares and a single stallion may enhance reproductive success by reducing aggression between individuals. Therefore, we propose that there is strong selection pressure for stable, long-term stallion-mare relationships, called consort relationships. We propose the consort hypothesis, that multistallion bands are an artefact of selection for stable relationships that occasionally result in more than one such relationship forming, because mares solicit more than one stallion and stallion dominance changes during band formation. Copyright 1999 The Association for the Study of Animal Behaviour.

Adaptive explanation in socio‐ecology: lessons from the Equidae

Socio‐ecological explanations for intra‐ and interspecific variation in the social and spatial organization of animals predominate in the scientific literature. The socio‐ecological model, developed first for the Bovidae and Cervidae, is commonly applied more widely to other groups including the Equidae. Intraspecific comparisons are particularly valuable because they allow the role of environment and demography on social and spatial organization to be understood while controlling for phylogeny or morphology which confound interspecific comparisons. Feral horse (Equus caballus Linnaeus 1758) populations with different demography inhabit a range of environments throughout the world. I use 56 reports to obtain 23 measures or characteristics of the behaviour and the social and spatial organization of 19 feral horse populations in which the environment, demography, management, research effort and sample size are also described. Comparison shows that different populations had remarkably similar social and spatial organization and that group sizes and composition, and home range sizes varied as much within as between populations. I assess the few exceptions to uniformity and conclude that they are due to the attributes of the studies themselves, particularly to poor definition of terms and inadequate empiricism, rather than to the environment or demography per se. Interspecific comparisons show that equid species adhere to their different social and spatial organizations despite similarities in their environments and even when species are sympatric. Furthermore, equid male territoriality has been ill‐defined in previous studies, observations presented as evidence of territoriality are also found in non‐territorial equids, and populations of supposedly territorial species demonstrate female defence polygyny. Thus, territoriality may not be a useful categorization in the Equidae. Moreover, although equid socio‐ecologists have relied on the socio‐ecological model derived from the extremely diverse Bovidae and Cervidae for explanations of variation in equine society, the homomorphic, but large and polygynous, and monogeneric Equidae do not support previous socio‐ecological explanations for relationships between body size, mating system and sexual dimorphism in ungulates. Consequently, in spite of the efforts of numerous authors during the past two decades, functional explanations of apparent differences in feral horse and equid social and spatial organization and behaviour based on assumptions of their current utility in the environmental or demographic context remain unconvincing. Nevertheless, differences in social cohesion between species that are insensitive to intra‐ and interspecific variation in habitat and predation pressure warrant explanation. Thus, I propose alternative avenues of inquiry including testing for species‐specific differences in inter‐individual aggression and investigating the role of phylogenetic constraints in equine society. The Equidae are evidence of the relative importance of phylogeny and biological structure, and unimportance of the present‐day environment, in animal behaviour and social and spatial organization.

Aging and improving reproductive success in horses: declining residual reproductive value or just older and wiser?

Abstractu2002In many mammalian species, female success in raising offspring improves as they age. The residual reproductive value hypothesis predicts that each individual offspring will be more valuable to the mother as she ages because there is less conflict between the current and potential future offspring. Therefore, as mothers age, their investment into individual offspring should increase. Empirical evidence for an influence of declining residual reproductive value on maternal investment is unconvincing. Older mothers may not invest more, but may be more successful due to greater experience, allowing them to target their investment more appropriately (targeted reproductive effort hypothesis). Most studies do not preclude either hypothesis. Mare age significantly influenced maternal investment in feral horses living on the North Island of New Zealand. Older mares, that were more successful at raising foals, were more protective for the first 20 days of life, but less diligent thereafter. Total maternal input by older mothers did not seem to be any greater, but was better targeted at the most critical period for foal survival and a similar pattern was observed in mares that had lost a foal in the previous year. In addition, older mothers were more likely to foal in consecutive years, supporting the hypothesis that they are investing less than younger mares in individual offspring. Therefore, older mothers seem to become more successful by targeting their investment better due to experience, not by investing more in their offspring.

Eye-Tracking of Men’s Preferences for Waist-to-Hip Ratio and Breast Size of Women

Studies of human physical traits and mate preferences often use questionnaires asking participants to rate the attractiveness of images. Female waist-to-hip ratio (WHR), breast size, and facial appearance have all been implicated in assessments by men of female attractiveness. However, very little is known about how men make fine-grained visual assessments of such images. We used eye-tracking techniques to measure the numbers of visual fixations, dwell times, and initial fixations made by men who viewed front-posed photographs of the same woman, computer-morphed so as to differ in her WHR (0.7 or 0.9) and breast size (small, medium, or large). Men also rated these images for attractiveness. Results showed that the initial visual fixation (occurring within 200xa0ms from the start of each 5xa0s test) involved either the breasts or the waist. Both these body areas received more first fixations than the face or the lower body (pubic area and legs). Men looked more often and for longer at the breasts, irrespective of the WHR of the images. However, men rated images with an hourglass shape and a slim waist (0.7 WHR) as most attractive, irrespective of breast size. These results provide quantitative data on eye movements that occur during male judgments of the attractiveness of female images, and indicate that assessments of the female hourglass figure probably occur very rapidly.

Extreme sex ratio variation in relation to change in condition around conception

Adaptive theory predicts that mothers would be advantaged by adjusting the sex ratio of their offspring in relation to their offsprings future reproductive success. Studies investigating sex ratio variation in mammals have produced notoriously inconsistent results, although recent studies suggest more consistency if sex ratio variation is related to maternal condition at conception, potentially mediated by changes in circulating glucose level. Consequently, we hypothesized that change in condition might better predict sex ratio variation than condition per se. Here, we investigate sex ratio variation in feral horses (Equus caballus), where sex ratio variation was previously shown to be related to maternal condition at conception. We used condition measures before and after conception to measure the change in condition around conception in individual mothers. The relationship with sex ratio was substantially more extreme than previously reported: 3% of females losing condition gave birth to a son, whereas 80% of those females that were gaining condition gave birth to a son. Change in condition is more predictive of sex ratio than actual condition, supporting previous studies, and shows the most extreme variation in mammals ever reported.

Suckling behaviour does not measure milk intake in horses, Equus caballus

Studies of parental investment in mammals have frequently used suckling behaviour to estimate energy transfer from mother to offspring, and consequently to measure maternal input. Such studies assume that the more an offspring sucks, the more milk it will receive. This assumption has been questioned, and a review of the literature found little support for it. To test if suckling behaviour provided an accurate index of milk or energy intake we used a radioactive isotope technique to label the milk of thoroughbred mares and to measure milk transfer to foals. We found no significant linear relationship between usual measures of suckling behaviour and milk or energy intake. No behaviours associated with suckling nor with characteristics of mares and foals improved the relationship; only the number of butts associated with each suck episode even approached significance. If we had used suckling behaviour to test theories on differential maternal investment our conclusions would have been in error. For example, female foals tended to suck for longer than males did but there was no difference in the amount of milk transferred. Consequently, we show that measures of suckling behaviour do not adequately predict milk intake in the domestic horse and we suggest that conclusions about differential maternal investment in mammals based on suckling behaviour are likely to be in error. Copyright 1999 The Association for the Study of Animal Behaviour.

Individual mares bias investment in sons and daughters in relation to their condition.

The Trivers-Willard hypothesis (TWH) predicts that a mother will treat a son or daughter differently depending on her ability to invest and the impact of her investment on offspring reproductive success. Although many studies have investigated the hypothesis, few have definitively supported or refuted it because of confounding factors or an inappropriate level of analysis. We studied maternal investment in sons and daughters in feral horses, Equus caballus, which meet the assumptions of the TWH with a minimum of confounding variables. Population level analyses revealed no differences in maternal behaviour towards sons and daughters. When we incorporated mare condition, we found that sons were more costly to mares in good condition, whereas daughters were more costly to mares in poor condition, although no differences in maternal behaviour were found. However, since the TWH makes predictions about individual mothers, we examined investment by mares who reared both a son and a daughter in different years of the study. Mares in good condition invested more in their sons in terms of maternal care patterns, costs to maternal body condition and costs to future reproduction. Conversely, mares in poor condition invested more in daughters. Therefore, with an appropriate level of analysis in a species in which confounding variables are minimal, the predictions of the Trivers-Willard hypothesis are supported. Copyright 2000 The Association for the Study of Animal Behaviour.

Social grouping and maternal behaviour in feral horses (Equus caballus): the influence of males on maternal protectiveness

Abstract. The risk of infant injury or mortality influences maternal behaviour, particularly protectiveness. Mares are found in bands with a single stallion or bands with more than one stallion in which paternity is less certain. We investigated maternal behaviour in relation to band type. Mares in bands with more than one stallion were more protective of their foals, particularly when stallions and foals approached one another. The rate of aggression between the stallion and foal was a significant predictor of maternal protectiveness, and mare protectiveness was significantly correlated with reduced reproductive success in the subsequent year. Mares that changed band types with a foal at foot, or had their band type experimentally altered, were more protective of their foal in multi-stallion bands than they were in single-stallion bands. Equids are unusual amongst ungulates in that infanticide and feticide have been reported. Both occur where paternity has been uncertain, and equid social structure is similar to other species in which infanticide has been reported. Stallions benefit from infanticide as the mare has greater reproductive success in the subsequent year. Stallion aggression is a significant modifier of mare behaviour and maternal effort, probably due to the risk of infanticide.

Sex bias in studies of sex bias: the value of daughters to mothers in poor condition

Confusion and, therefore, controversy still surrounds the predictions of Trivers & Willard (1973) and the conclusions of later empirical tests (e.g. Festa-Bianchet 1996), despite the relative simplicity of the original model (the Trivers–Willard hypothesis, or TWH, Table 1). We welcome the conclusion that a ‘greater integration of empirical and theoretical work on the TW hypothesis is needed’ (Carranza 2002). None the less, to comprehend the TWH, and at least partially to resolve the confusion, it is necessary to consider, as Carranza suggests in his title, what did Trivers and Willard really predict? The TWH was originally a verbal model as Carranza correctly notes. Nevertheless, Trivers & Willard (1973) were explicit about the assumptions of their model, its predictions and in their use of the existing literature to support their hypothesis. The primary issue raised by Carranza is whether the TWH predicted that daughters would be favoured under certain circumstances and whether this is feasible. The TWH is explicit in predicting that investing more in daughters than sons will advantage mothers in poor condition. When summarizing their hypothesis, Trivers & Willard stated that ‘an adult female in poor condition who produces a daughter will leave more surviving grandchildren than a similar female who produces a son’. This is further supported by their statement that ‘these deviations tend to cancel out in the local breeding population’. If mothers in good condition were giving birth to significantly more sons, the breeding population could only produce a 50/50 birth sex ratio, as observed in horses, Equus caballus (Cameron et al. 1999), if all other mothers produced more daughters than sons. The importance of female-biased sex ratios in mothers in poor condition is underscored in Trivers & Willard’s discussion of empirical data. They spent almost an entire column in a five-column article discussing the phenomenon of differential loss of sons in utero by mothers in poor condition. Second, Carranza questions whether the TWH predictions can be extended to maternal investment. If we are simply considering what ‘Trivers and Willard really predict’ then it is clear that the TWH predicts variation in maternal investment as well as sex ratios. Trivers & Willard (1973) stated ‘one might expect biases in parental behaviour toward offspring of different sex, according to parental condition: parents in better condition would be expected to invest more in male offspring’. Carranza suggests that, at best, this statement makes predictions about bias in investment into sons. On the contrary we think it is explicit in its application to both sexes by stating that there should be ‘biases in parental behaviour toward offspring of different sex, according to parental condition’. Trivers & Willard (1973) were careful not to confine their terminology to males only. Therefore, our interpretation of TWH is that there are two explicit predictions and these apply to both sex ratios and maternal investment. (1) Mothers in better condition would be favoured by producing more sons (than daughters) and investing more in sons (than daughters). (2) Mothers in poorer condition would be favoured by producing more daughters (than sons) and investing more in daughters (than sons). Mothers following these strategies would leave more grandchildren than mothers that did not (Trivers & Willard 1973). Many studies on maternal investment overlook the prediction that mothers in poorer condition would be advantaged by investing more in daughters and Correspondence: E. Z. Cameron, Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa (email: ezcameron@zoology.up.ac.za). W. L. Linklater is at the Center for Reproduction of Endangered Species, Zoological Society of San Diego, P.O. Box 120551, San Diego, California 92112-0551, U.S.A.