Ann MacLarnon

A phylogenetic supertree of the bats (Mammalia: Chiroptera).

We present the first estimate of the phylogenetic relationships among all 916 extant and nine recently extinct species of bats (Mammalia: Chiroptera), a group that accounts for almost one‐quarter of extant mammalian diversity. This phylogeny was derived by combining 105 estimates of bat phylogenetic relationships published since 1970 using the supertree construction technique of Matrix Representation with Parsimony (MRP). Despite the explosive growth in the number of phylogenetic studies of bats since 1990, phylogenetic relationships in the order have been studied non‐randomly. For example, over one‐third of all bat systematic studies to date have focused on relationships within Phyllostomidae, whereas relationships within clades such as Kerivoulinae and Murinae have never been studied using cladistic methods. Resolution in the supertree similarly differs among clades: overall resolution is poor (46.4% of a fully bifurcating solution) but reaches 100% in some groups (e.g. relationships within Mormoopidae). The supertree analysis does not support a recent proposal that Microchiroptera is paraphyletic with respect to Megachiroptera, as the majority of source topologies support microbat monophyly. Although it is not a substitute for comprehensive phylogenetic analyses of primary molecular and morphological data, the bat supertree provides a useful tool for future phylogenetic comparative and macroevolutionary studies. Additionally, it identifies clades that have been little studied, highlights groups within which relationships are controversial, and like all phylogenetic studies, provides preliminary hypotheses that can form starting points for future phylogenetic studies of bats.

The evolution of human speech: the role of enhanced breathing control.

Many cognitive and physical features must have undergone change for the evolution of fully modern human language. One neglected aspect is the evolution of increased breathing control. Evidence presented herein shows that modern humans and Neanderthals have an expanded thoracic vertebral canal compared with australopithecines and Homo ergaster, who had canals of the same relative size as extant nonhuman primates. Based on previously published analyses, these results demonstrate that there was an increase in thoracic innervation during human evolution. Possible explanations for this increase include postural control for bipedalism, increased difficulty of parturition, respiration for endurance running, an aquatic phase, and choking avoidance. These can all be ruled out, either because of their evolutionary timing, or because they are insufficiently demanding neurologically. The remaining possible functional cause is increased control of breathing for speech. The main muscles involved in the fine control of human speech breathing are the intercostals and a set of abdominal muscles which are all thoracically innervated. Modifications to quiet breathing are essential for modern human speech, enabling the production of long phrases on single expirations punctuated with quick inspirations at meaningful linguistic breaks. Other linguistically important features affected by variation in subglottal air pressure include emphasis of particular sound units, and control of pitch and intonation. Subtle, complex muscle movements, integrated with cognitive factors, are involved. The vocalizations of nonhuman primates involve markedly less respiratory control. Without sophisticated breath control, early hominids would only have been capable of short, unmodulated utterances, like those of extant nonhuman primates. Fine respiratory control, a necessary component for fully modern language, evolved sometime between 1.6 Mya and 100,000 ya.

Grooming in Barbary macaques: better to give than to receive?

It is well established that grooming underpins sociality in group-living primates, and a number of studies have documented the stress-reducing effects of being groomed. In this study, we quantified grooming behaviour and physiological stress (assessed by faecal glucocorticoid analysis) in free-ranging Barbary macaques, Macaca sylvanus. Our results indicate that it is the giving rather than the receiving of grooming that is associated with lower stress levels. These findings shed important new light on the benefits of this key behaviour in primate social life.

Baboon sexual swellings: Information content of size and color

Primate sexual swellings are hormone-dependent sexual signals that play a key role in determining patterns of behavior. They are among the most conspicuous signals exhibited by any mammal, and their large size and bright coloration have fascinated evolutionary biologists for well over a century. A number of different adaptive hypotheses have been proposed for the evolution of sexual swellings, and there have been several recent attempts to test some of these using precise swelling measurements made in the field. Most of these studies have focused only on the size element of the swelling, and those that have measured other aspects of swellings, such as color, have done so only crudely. A focus solely on swelling size is inconsistent with most theoretical models of mate choice, which emphasize the importance of multiple cues within sexual signals. Here, we present data on baboon (Papio hamadryas anubis) sexual swellings, including measures of both swelling size and color, measured objectively using digital photography at Gashaka-Gumti National Park, Nigeria. We combined these measurements with detailed data on fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period around ovulation based on those levels. We show that swelling color and size vary independently, and that, consistent with results in other species, swelling size contains information about the timing of ovulation and the fertile period. However, we show that swelling color does not contain such information. In addition, swelling size contains information about female parity, and we found some evidence to suggest that color may also contain such information. These results indicate that baboon sexual swellings may contain information about multiple aspects of female fertility. We discuss the implications of these results for understanding the nature of swellings as behavioral signals, and the role of swellings in mate choice.

The Evolution of Non-Maternal Care in Anthropoid Primates: A Test of the Hypotheses

The amount of non-maternal care (allocare) found in primates varies greatly from species to species. Our paper examines this variation and focuses on possible reasons why mothers in some anthropoid primate species are prepared to relinquish their infants to other carers whereas others are not. We use data collected from the literature to test a number of hypotheses that attempt to explain the observed variation in non-maternal care. Analyses were carried out using comparative methods that control for the influence of both body size and phylogeny on life-history and ecological variation. The results support previous studies of both primates and other mammals in finding a clear link between the amount of allocare provided and female reproductive rates. Species with high allocare levels grow rapidly post-natally and wean their infants at a younger age (but at the same relative size) than species of the same body size with lower allocare levels. This early weaning allows high allocare species to support higher birth rates than low allocare species but does not result in earlier maturation. Our results, therefore, suggest that mothers allow non-maternal care of their infants in order to increase their own reproductive output. It is not clear whether such a strategy also benefits the infant, as we could find no link between the presence of allocare and early maturation (which would increase the infant’s reproductive output) or between allocare levels and infant survival (as measured by vulnerability to infanticide). This suggests that mothers and infants might come into conflict over transfer to other carers, as the benefits to the mother may not be accompanied by benefits to the infant. However, although mothers may benefit from allocare in some circumstances, they will not be expected to allow allocare if the costs are high (e.g. if there is a high risk to the infant).

Sexual Skin Color Contains Information About the Timing of the Fertile Phase in Free-ranging Macaca mulatta

Females of several primate species undergo cyclical changes of their sexual skin, i.e., the development of a swelling or a change in color. The relationship between intracycle probability of fertility and the size of sexual swellings is well established, but in the only study to combine an objective measure of color with endocrinological data, researchers found no evidence that swelling color contains such information. To evaluate the role of female skin color in the context of sexual signaling further, we investigated whether changes in sexual skin color contain information about the timing of the fertile phase in rhesus macaques (Macaca mulatta), a species in which adult females do not develop sexual swellings, but do express visually detectable changes in the skin color of the face and hindquarters. Using an objective and quantitative measure of color, along with detailed data on fecal progestogen and estrogen metabolite levels collected from 8 females of the Cayo Santiago colony, we show that the ratio of red to green (R/G) for facial and hindquarter skin significantly varies throughout the ovarian cycle. In addition, facial skin R/G is significantly higher during the 5-d fertile phase versus the 5-d periods immediately before or after this time, but no such pattern occurs in hindquarter R/G. This suggests that skin color change in female rhesus macaques may potentially signal information about the intracycle probability of fertility to male receivers, but that only facial skin color may signal reliable information about its timing.

The Functions of Laryngeal Air Sacs in Primates: A New Hypothesis

A possible function of laryngeal air sacs in apes and gibbons was investigated by examining the relationships between air sac distribution, call rate, call duration and body weight in a phylogenetic context. The results suggest that lack of sacs in the smaller gibbons and in humans is a derived feature. Call parameters in primates, such as rate and duration, scaled to resting breathing rate (and therefore to body weight) only in species without air sacs, which appear to modify these relationships. Apes and larger gibbons may be able to produce fast extended call sequences without the risk of hyperventilating because they can re-breathe exhaled air from their air sacs. Humans may have lost air sacs during their evolutionary history because they are able to modify their speech breathing patterns and so reduce any tendency to hyperventilate.

Gastrointestinal Allometry in Primates and Other Mammals

There has been a considerable upsurge of interest recently in the concept of interspecific allometry (Gould, 1966), which relates to the scaling of individual characteristics to match body size in different species. Two particularly important developments have been taking place in theoretical aspects of allometry (e.g., see other contributions to this volume) and in the extension of allometric analysis to new fields of enquiry. One example of the application of allometric principles to an entirely new area of research is provided by the work conducted by Chivers and Hladik (1980) on the morphology of the gastrointestinal tract in primates and other mammals. Further development of this particular approach forms the subject of this chapter.

Affording larger brains: testing hypotheses of mammalian brain evolution on bats.

Several major hypotheses have been proposed to explain how larger brains in mammals, such as those of humans, are afforded in energetic terms. To date, these have been largely tested on primates, with some cross‐mammal analysis. We use morphological, ecological, and metabolic data for 313 species of bats to examine the allometry of brain mass and to test key predictions from three of these hypotheses: the direct metabolic constraint, expensive tissue, and maternal energy hypotheses. We confirm that megachiropteran bats (entirely fruit‐eating) have larger brains for their body mass than microchiropteran bats (fruit‐eating and non‐fruit‐eating) and fruit‐eating species (Megachiroptera and Microchiroptera) have larger brains than non‐fruit‐eating species (Microchiroptera). Although our analyses demonstrate little or no support for any of the three hypotheses, we show that 95.9% of the variance in brain mass can be explained by the independent effects of gestation length and body mass. This indicates that among bats, the duration of maternal investment plays an important role in the adult brain mass finally obtained. These analyses serve to emphasis the crucial importance of testing the general applicability of macroevolutionary hypotheses (often developed in isolation in one clade) in multiple clades with different evolutionary histories.

Social capital and physiological stress levels in free-ranging adult female rhesus macaques.

Social animals with greater access to social support, i.e. higher levels of social capital, may be able to cope better with the challenges they face in their day-to-day lives, and this may be reflected in lower physiological stress levels. Here, we examine the relationship between social capital and fecal glucocorticoid (GC) levels in pregnant free-ranging adult female rhesus macaques. In addition to social capital measures based on direct connections between social partners, which have been examined previously, we use social network analysis to generate measures of social capital based on indirect connections (i.e. connections between pairs of individuals which result from their mutual direct connection to a third party). We consider social capital based on three different types of affiliative association: grooming, the exchange of affiliative vocalizations and proximity. After controlling for variables known to affect GC output in primates (e.g. month of pregnancy), GC levels of females were significantly predicted by a social network measure of indirect connectedness in the proximity network, proximity reach, in interaction with dominance rank. High ranking females had significantly lower GC levels in months in which they had low levels of proximity reach (i.e. in months in which their proximity networks were smaller and therefore more focused). The results of our study add to a growing body of evidence which suggests that social capital may be an important means by which gregarious animals cope with day-to-day challenges. Our study also joins a small body of recent research which has demonstrated that indirect connections may be important factors in the lives of social animals.