Ecological Knowledge, Leadership, and the Evolution of Menopause in Killer Whales

SummaryClassic life-history theory predicts that menopause should not occur because there should be no selection for survival after the cessation of reproduction [1]. Yet, human females routinely live 30 years after they have stopped reproducing [2]. Only two other species—killer whales (Orcinus orca) and short-finned pilot whales (Globicephala macrorhynchus) [3, 4]—have comparable postreproductive lifespans. In theory, menopause can evolve via inclusive fitness benefits [5, 6], but the mechanisms by which postreproductive females help their kin remain enigmatic. One hypothesis is that postreproductive females act as repositories of ecological knowledge and thereby buffer kin against environmental hardships [7, 8]. We provide the first test of this hypothesis using a unique long-term dataset on wild resident killer whales. We show three key results. First, postreproductively aged females lead groups during collective movement in salmon foraging grounds. Second, leadership by postreproductively aged females is especially prominent in difficult years when salmon abundance is low. This finding is critical because salmon abundance drives both mortality and reproductive success in resident killer whales [9, 10]. Third, females are more likely to lead their sons than they are to lead their daughters, supporting predictions of recent models [5] of the evolution of menopause based on kinship dynamics. Our results show that postreproductive females may boost the fitness of kin through the transfer of ecological knowledge. The value gained from the wisdom of elders can help explain why female resident killer whales and humans continue to live long after they have stopped reproducing

Sociality predicts individual variation in the immunity of free-ranging rhesus macaques

This work was supported by CONICYT-Chilean scholarship [number 72190290], NIH grant [number R01AG060931] to N.S-M., L.J.N.B. and J.P.H., NIH grant [number R00AG051764] to N.S-M., NIH grant [number MH118203] to L.J.N.B.. and M.L.P, and NSF grant [number 1800558] to J.P.H. and Susan Anton. The CPRC is supported by the National Institutes of Health. An Animal and Biological Material Resource Center Grant [P40OD012217] was awarded to UPR from the Office of Research Infrastructure Programs (ORIP), and a Research Facilities Construction Grant [C06OD026690] was awarded for the renovation of CPRC facilities after Hurricane Maria.Social integration and social status can substantially affect an individual's health and survival. One route through which this occurs is by altering immune function, which can be highly sensitive to changes in the social environment. However, we currently have limited understanding of how sociality influences markers of immunity in naturalistic populations where social dynamics can be fully realized. To address this gap, we asked if social integration and social status in free-ranging rhesus macaques (Macaca mulatta) predict anatomical and physiological markers of immunity. We used data on agonistic interactions to determine social status, and social network analysis of grooming interactions to generate measures of individual variation in social integration. As measures of immunity, we included the size of two of the major organs involved in the immune response, the spleen and liver, and counts of three types of blood cells (red blood cells, platelets, and white blood cells). Controlling for body mass and age, we found that neither social status nor social integration predicted the size of anatomical markers of immunity. However, individuals that were more socially connected, i.e., with more grooming partners, had lower numbers of white blood cells than their socially isolated counterparts, indicating lower levels of inflammation with increasing levels of integration. These results build upon and extend our knowledge of the relationship between sociality and the immune system in humans and captive animals to free-ranging primates, demonstrating generalizability of the beneficial role of social integration on health.Publisher PDFPeer reviewe

Trade-offs between sociality and gastrointestinal parasite infection in the context of a natural disaster

This work was supported by ANID-Chilean scholarship [number 72190290], the National Institutes of Health Grants [R01AG060931] to N.S-M., L.J.N.B. and J.P.H., [R00AG051764] to N.S-M, [R01MH118203] to M.L.P., M.J.M, L.J.N.B. and N.S-M., [R01MH096875] to M.L.P., L.J.N.B. and M.J.M., [U01MH121260] to N.S-M., M.L.P. and M.J.M., a European Research Council Consolidator Grant to L.J.N.B. [Friend Origins - 864461].Parasites and infectious diseases constitute important challenges particularly for group-living animals. Social contact and shared space can both increase parasite transmission risk, while individual differences in social capital can help prevent infections. For example, high social status individuals and those with more or stronger affiliative partnerships may have better immunity and, thus, lower parasitic burden. To test for health trade-offs in the costs and benefits of sociality, we quantified how parasitic load varied with an individual's social status, as well as with their affiliative relationships with weakly and strongly bonded partners, in a free-ranging population of rhesus macaques, Macaca mulatta. We found that high status was associated with a lower risk of protozoa infection at older ages compared to younger and low-status animals. Social resources can also be protective against infection under environmentally challenging situations, such as natural disasters. Using cross-sectional data, we additionally examined the impact of a major hurricane on the sociality - parasite relationship in this system and found that the hurricane influenced the prevalence of specific parasites independent of sociality. Overall, our study adds to the growing evidence for social status as a strong predictor of infection risk and highlights how extreme environmental events could shape vulnerability and resistance to infection.Peer reviewe

Sociality predicts individual variation in the immunity of free-ranging rhesus macaques

This is the final version. Available from Elsevier via the DOI in this record. R- code used for models and plots available at https://github.com/MPavFox/Sociality-and-Immunity-rhesus.gitSocial integration and social status can substantially affect an individual's health and survival. One route through which this occurs is by altering immune function, which can be highly sensitive to changes in the social environment. However, we currently have limited understanding of how sociality influences markers of immunity in naturalistic populations where social dynamics can be fully realized. To address this gap, we asked if social integration and social status in free-ranging rhesus macaques (Macaca mulatta) predict anatomical and physiological markers of immunity. We used data on agonistic interactions to determine social status, and social network analysis of grooming interactions to generate measures of individual variation in social integration. As measures of immunity, we included the size of two of the major organs involved in the immune response, the spleen and liver, and counts of three types of blood cells (red blood cells, platelets, and white blood cells). Controlling for body mass and age, we found that neither social status nor social integration predicted the size of anatomical markers of immunity. However, individuals that were more socially connected, i.e., with more grooming partners, had lower numbers of white blood cells than their socially isolated counterparts, indicating lower levels of inflammation with increasing levels of integration. These results build upon and extend our knowledge of the relationship between sociality and the immune system in humans and captive animals to free-ranging primates, demonstrating generalizability of the beneficial role of social integration on health.National Institutes of HealthNational Institute for Mental Health ResearchCONICYT-Chilean scholarshipNational Institute of HealthAnimal and Biological Material Resource Cente

Large expert-curated database for benchmarking document similarity detection in biomedical literature search

Document recommendation systems for locating relevant literature have mostly relied on methods developed a decade ago. This is largely due to the lack of a large offline gold-standard benchmark of relevant documents that cover a variety of research fields such that newly developed literature search techniques can be compared, improved and translated into practice. To overcome this bottleneck, we have established the RElevant LIterature SearcH consortium consisting of more than 1500 scientists from 84 countries, who have collectively annotated the relevance of over 180 000 PubMed-listed articles with regard to their respective seed (input) article/s. The majority of annotations were contributed by highly experienced, original authors of the seed articles. The collected data cover 76% of all unique PubMed Medical Subject Headings descriptors. No systematic biases were observed across different experience levels, research fields or time spent on annotations. More importantly, annotations of the same document pairs contributed by different scientists were highly concordant. We further show that the three representative baseline methods used to generate recommended articles for evaluation (Okapi Best Matching 25, Term Frequency-Inverse Document Frequency and PubMed Related Articles) had similar overall performances. Additionally, we found that these methods each tend to produce distinct collections of recommended articles, suggesting that a hybrid method may be required to completely capture all relevant articles. The established database server located at https://relishdb.ict.griffith.edu.au is freely available for the downloading of annotation data and the blind testing of new methods. We expect that this benchmark will be useful for stimulating the development of new powerful techniques for title and title/abstract-based search engines for relevant articles in biomedical research.Peer reviewe

Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output

There is growing evidence that behavioral tendencies, or “personalities,” in animals are an important aspect of their biology, yet their evolutionary basis is poorly understood. Specifically, how individual variation in personality arises and is subsequently maintained by selection remains unclear. To address this gap, studies of personality require explicit incorporation of genetic information. Here, we explored the genetic basis of personality in rhesus macaques by determining the heritability of personality components and by examining the fitness consequences of those components. We collected observational data for 108 adult females living in three social groups in a free-ranging population via focal animal sampling. We applied principal component analysis to nine spontaneously occurring behaviors and identified six putative personality components, which we named Meek, Bold, Aggressive, Passive, Loner, and Nervous. All components were repeatable and heritable, with heritability estimates ranging from 0.14 to 0.35. We found no evidence of an association with reproductive output, measured either by infant survival or by interbirth interval, for any of the personality components. This finding suggests either that personality does not have fitness-related consequences in this population or that selection has acted to reduce fitness-associated variation in personality

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