Christine M. Drea

How does cognition evolve? Phylogenetic comparative psychology

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.

Influence of early photoreceptor degeneration on lipofuscin in the retinal pigment epithelium

Experiments were conducted to evaluate the role played by photoreceptor cells in the accumulation of age pigment, or lipofuscin, in the retinal pigment epithelium (RPE). The age-related accumulation of RPE lipofuscin was compared between rats with hereditary photoreceptor degeneration (RDY) and congenic rats with normal retinas. In the RDY animals, the age-related increase in RPE lipofuscin content was substantially less than in normal controls. This suggests that the photoreceptor cells play a significant role in RPE lipofuscin deposition, although they may not be the sole contributors to RPE lipofuscin formation. Evidence that outer-segment components may be converted into lipofuscin fluorophores was provided by the discovery that in young RDY rats, fragments of outer segments from degenerating photoreceptor cells had fluorescence properties similar to those of RPE lipofuscin. Chloroform-methanol extraction of retina-RPE tissue from young normal and dystrophic rats, and analysis of the chloroform fractions by thin-layer chromatography, revealed three distinct fluorescent components associated with the lipofuscin-like fluorescence of the outer-segment fragments in the RDY rats.

Smelling right: the scent of male lemurs advertises genetic quality and relatedness

Sexual selection theory predicts that competitors or potential mates signal their quality or relatedness to conspecifics. Researchers have focused on visual or auditory modes of signal transmission; however, the importance of olfactory indicators is gaining recognition. Using a primate model and a new integrative analytical approach, we provide the first evidence relating male olfactory cues to individual genome‐wide heterozygosity and to the genetic distance between individuals. The relationships between male semiochemical profiles and genetic characteristics are apparent only during the highly competitive and stressful breeding season. As heterozygosity accurately predicts health and survivorship in this population, we identify scrotal olfactory cues as honest indicators of male quality, with relevance possibly to both sexes. Beyond showing that semiochemicals could underlie kin recognition and nepotism, we provide a putative olfactory mechanism to guide male–male competition and female mate choice.

Cooperative problem solving in a social carnivore

Numerous field researchers have described cooperative hunting in social carnivores, but experimental evidence of cooperative problem solving typically derives from laboratory studies of nonhuman primates. We present the first experimental evidence of cooperation in a social carnivore, the spotted hyaena, Crocuta crocuta. Eight captive hyaenas, paired in 13 combinations, coordinated their behaviour temporally and spatially to solve cooperation tasks that modelled group-hunting strategies. Unlike many primates that cooperate infrequently or require extensive shaping, spotted hyaenas displayed a natural aptitude for teamwork: all teams achieved success rapidly, repeatedly, and without specific training. Social influences on cooperative performance included an audience effect that could influence party formation and hunting success in the wild. Performance also varied across dyads, notably with rank-related aggression between partners impairing performance. Efficiency improved as partners increasingly attended to one another and coordinated their actions. Lastly, experienced cooperators modified their behaviour to accommodate a naive companion, using visual monitoring and tracking to promote coordination. We suggest that social carnivores should be considered relevant models for the study of cooperative problem solving, as their abilities provide a comparative framework for testing theories about the mechanisms of social learning and the evolution of intelligence.

Message ‘scent’: lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues

To enhance the fitness benefits of social and sexual interaction, animals should be able to decipher information about the genetic makeup of conspecifics. The use of relative criteria to estimate genetic relatedness could facilitate nepotism or inbreeding avoidance, and the use of absolute criteria to estimate genetic quality could help identify the fittest competitor or the best mate. For animals to process trade-offs between relatedness and quality, however, both relative and absolute genetic information must be concurrently available and detectable by conspecifics. Although there is increasing evidence to suggest that animals make genetically informed decisions about their partners, and may even process trade-offs, we understand relatively little about the sensory mechanisms informing these decisions. In previous analyses of the olfactory signals of ringtailed lemurs, Lemur catta, we showed that both scrotal and labial secretions seasonally encode chemical information about (1) pairwise genetic relatedness, within and between the sexes, and (2) individual heterozygosity. Here, using a signaller–receiver paradigm, we conducted behavioural bioassays to test whether male and female lemurs are sensitive to these olfactory sources of genetic information in unfamiliar conspecifics. As the lemurs discriminated conspecific glandular secretions by pairwise relatedness and individual heterozygosity, volatile olfactory signals can be used by both sexes to concurrently process relative and absolute genetic information about conspecifics. Beyond supporting an olfactory mechanism of kin discrimination and mate choice in a primate, we suggest that animals could use olfactory processing to trade off between selection for the most compatible partner versus the most genetically diverse partner.

Asymmetrical Hand Use in Rhesus Monkeys (Macaca mulatta) in Tactually and Visually Regulated Tasks

Asymmetrical hand use by rhesus monkeys (Macaca mulatta) was investigated in a series of tactually and visually guided tasks. The 1st experiment recorded manual preferences of 29 monkeys for solving a haptic discrimination task in a hanging posture. There was a left-hand population bias: 21 monkeys had a left-hand bias, 4 a right-hand bias, and 4 no bias. The 2nd experiment, 4 tasks with 23 to 51 monkeys, investigated the critical components of the 1st experiment by varying the posture (hanging, sitting, or tripedal) and the sensory requirements (tactile or visual). Posture influenced hand bias, with a population-level left-hand bias in hanging and sitting postures, but an almost symmetrical distribution in the tripedal posture. A left-hand bias was found for both sensory modalities, but the bias was stronger in the tactual tasks. Results suggest a possible right-hemisphere specialization in the rhesus for tactile, visual, or spatial processing.

Relationship between dietary retinol and lipofuscin in the retinal pigment epithelium

A variety of evidence suggests that autoxidation of cellular components probably plays a significant role in the age-related accumulation of lipofuscin, or age-pigment, in the mammalian retinal pigment epithelium (RPE). Among the likely candidates for conversion into RPE lipofuscin fluorophores via autoxidative mechanisms are vitamin A compounds, which are present in the retina and RPE in high concentrations. Vitamin E, an important lipid antioxidant, is likely to inhibit vitamin A autoxidation. Experiments were conducted to evaluate the significance of vitamin A autoxidation in the deposition of lipofuscin in the RPE. Albino rats were fed diets either supplemented with or lacking vitamin E. Each of these two groups of animals was further subdivided into three groups which were fed different levels of vitamin A palmitate: none, 14.0 mumol/kg diet, and 80.5 mumol/kg diet. After 26 weeks, the animals were killed and the RPE lipofuscin contents were determined by both fluorescence measurements and quantitative ultrastructural morphometry. Vitamin A palmitate deficiency led to significant reductions in RPE lipofuscin deposition, relative to the amounts of this pigment present in the groups receiving vitamin A palmitate in their diets. The relative magnitude of the vitamin A effect was greater in the vitamin E-supplemented groups than in the groups fed the diets deficient in vitamin E. This finding suggests that vitamin E interacts with vitamin A ester metabolites in vivo in a more complex manner than simply acting as an antioxidant protectant. Rats fed the diets containing the higher level of vitamin A palmitate failed to display elevated RPE lipofuscin contents relative to those in the rats fed 14.0 mumol of vitamin A palmitate/kg diet. Failure of high vitamin A intake to enhance RPE lipofuscin deposition may have been due to the fact that intake of vitamin A above normal levels did not lead to an elevation in vitamin A content of the retinal tissue. Establishing an effect of vitamin A deficiency on RPE lipofuscin deposition and characterization of the interactions between vitamins E and A are important steps toward defining precisely the molecular and cellular mechanisms underlying age-pigment accumulation in the RPE.

Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate

BackgroundLike other vertebrates, primates recognize their relatives, primarily to minimize inbreeding, but also to facilitate nepotism. Although associative, social learning is typically credited for discrimination of familiar kin, discrimination of unfamiliar kin remains unexplained. As sex-biased dispersal in long-lived species cannot consistently prevent encounters between unfamiliar kin, inbreeding remains a threat and mechanisms to avoid it beg explanation. Using a molecular approach that combined analyses of biochemical and microsatellite markers in 17 female and 19 male ring-tailed lemurs (Lemur catta), we describe odor-gene covariance to establish the feasibility of olfactory-mediated kin recognition.ResultsDespite derivation from different genital glands, labial and scrotal secretions shared about 170 of their respective 338 and 203 semiochemicals. In addition, these semiochemicals encoded information about genetic relatedness within and between the sexes. Although the sexes showed opposite seasonal patterns in signal complexity, the odor profiles of related individuals (whether same-sex or mixed-sex dyads) converged most strongly in the competitive breeding season. Thus, a strong, mutual olfactory signal of genetic relatedness appeared specifically when such information would be crucial for preventing inbreeding. That weaker signals of genetic relatedness might exist year round could provide a mechanism to explain nepotism between unfamiliar kin.ConclusionWe suggest that signal convergence between the sexes may reflect strong selective pressures on kin recognition, whereas signal convergence within the sexes may arise as its by-product or function independently to prevent competition between unfamiliar relatives. The link between an individuals genome and its olfactory signals could be mediated by biosynthetic pathways producing polymorphic semiochemicals or by carrier proteins modifying the individual bouquet of olfactory cues. In conclusion, we unveil a possible olfactory mechanism of kin recognition that has specific relevance to understanding inbreeding avoidance and nepotistic behavior observed in free-ranging primates, and broader relevance to understanding the mechanisms of vertebrate olfactory communication.

Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating

Among all extant mammals, only the female spotted hyena (Crocuta crocuta) mates and gives birth through the tip of a peniform clitoris. Clitoral morphology is modulated by foetal exposure to endogenous, maternal androgens. First births through this organ are prolonged and remarkably difficult, often causing death in neonates. Additionally, mating poses a mechanical challenge for males, as they must reach an anterior position on the females abdomen and then achieve entry at the site of the retracted clitoris. Here, we report that interfering with the actions of androgens prenatally permanently modifies hyena urogenital anatomy, facilitating subsequent parturition in nulliparous females who, thereby, produce live cubs. By contrast, comparable, permanent anatomical changes in males probably preclude reproduction, as exposure to prenatal anti–androgens produces a penis that is too short and has the wrong shape necessary for insertion during copulation. These data demonstrate that the reproductive costs of clitoral delivery result from exposure of the female foetus to naturally circulating androgens. Moreover, the same androgens that render an extremely unusual and laborious process even more reproductively costly in the female are apparently essential to the males physical ability to reproduce with a normally masculinized female.

Honest olfactory ornamentation in a female-dominant primate

Sexual selection theory predicts that potential mates or competitors signal their quality to conspecifics. Whereas evidence of honest visual or vocal signals in males abounds, evidence of honest signalling via scent or by females is scarce. We previously showed that scent marks in male lemurs seasonally encode information about individual heterozygosity – a reliable predictor of immunocompetence and survivorship. As female lemurs dominate males, compete over resources, and produce sexually differentiated scent marks that likely evolved via direct selection, here we tested whether females also advertise genetic quality via olfactory cues. During the breeding season specifically, individual heterozygosity correlated negatively with the diversity of fatty acids (FAs) expressed in labial secretions and positively with the diversity of heavy FA esters. As odour–gene relationships predictive of health and survivorship emerged during a period critical to mate choice and female competition, we posit that genital scent marks function as honest olfactory ornaments in females.