Social and endocrine correlates of immune function in meerkats: implications for the immunocompetence handicap hypothesis.

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in free-ranging animals have used faecal parasite burdens to proxy immune function in the males of male-dominant species. We instead use direct measures of innate immune function (complement and natural antibodies) to examine status-related immunocompetence in both sexes of a female-dominant species. The meerkat is a unique model for such a study because it is a cooperatively breeding species in which status-related differences are extreme, evident in reproductive skew, morphology, behaviour, communication and physiology, including that dominant females naturally express the greatest total androgen (androstenedione plus testosterone) concentrations. We found that, relative to subordinates, dominant animals had reduced serum bacteria-killing abilities; also, relative to subordinate females, dominant females had reduced haemolytic complement activities. Irrespective of an individual's sex or social status, androstenedione concentrations (but not body condition, age or reproductive activity) negatively predicted concurrent immunocompetence. Thus, dominant meerkats of both sexes are immunocompromised. Moreover, in female meerkats, androstenedione perhaps acting directly or via local conversion, may exert a double-edged effect of promoting dominance and reproductive success at the cost of increased parasitism and reduced immune function. Given the prominent signalling of dominance in female meerkats, these findings may relate to the immunocompetence handicap hypothesis (ICHH); however, our data would suggest that the endocrine mechanism underlying the ICHH need not be mediated solely by testosterone and might explain trade-offs in females, as well as in males

Exceptional endocrine profiles characterise the meerkat: sex, status, and reproductive patterns.

In vertebrates, reproductive endocrine concentrations are strongly differentiated by sex, with androgen biases typifying males and estrogen biases typifying females. These sex differences can be reduced in female-dominant species; however, even the most masculinised of females have less testosterone (T) than do conspecific males. To test if aggressively dominant, female meerkats (Suricata suricatta) may be hormonally masculinised, we measured serum androstenedione (A4), T and estradiol (E2) in both sexes and social classes, during both 'baseline' and reproductive events. Relative to resident males, dominant females had greater A4, equivalent T and greater E2 concentrations. Males, whose endocrine values did not vary by social status, experienced increased T during reproductive forays, linking T to sexual behaviour, but not social status. Moreover, substantial E2 concentrations in male meerkats may facilitate their role as helpers. In females, dominance status and pregnancy magnified the unusual concentrations of measured sex steroids. Lastly, faecal androgen metabolites replicated the findings derived from serum, highlighting the female bias in total androgens. Female meerkats are thus strongly hormonally masculinised, possibly via A4's bioavailability for conversion to T. These raised androgen concentrations may explain female aggressiveness in this species and give dominant breeders a heritable mechanism for their daughters' competitive edge

Social and endocrine correlates of immune function in meerkats : implications for the immunocompetence

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in freeranging animals have used faecal parasite burdens to proxy immune function in the males of male-dominant species. We instead use direct measures of innate immune function (complement and natural antibodies) to examine status-related immunocompetence in both sexes of a femaledominant species. The meerkat is a unique model for such a study because it is a cooperatively breeding species in which status-related differences are extreme, evident in reproductive skew, morphology, behaviour, communication and physiology, including that dominant females naturally express the greatest total androgen (androstenedione plus testosterone) concentrations. We found that, relative to subordinates, dominant animals had reduced serum bacteria-killing abilities; also, relative to subordinate females, dominant females had reduced haemolytic complement activities. Irrespective of an individual’s sex or social status, androstenedione concentrations (but not body condition, age or reproductive activity) negatively predicted concurrent immunocompetence. Thus, dominant meerkats of both sexes are immunocompromised. Moreover, in female meerkats, androstenedione perhaps acting directly or via local conversion, may exert a double-edged effect of promoting dominance and reproductive success at the cost of increased parasitism and reduced immune function. Given the prominent signalling of dominance in female meerkats, these findings may relate to the immunocompetence handicap hypothesis (ICHH); however, our data would suggest that the endocrine mechanism underlying the ICHH need not be mediated solely by testosterone and might explain trade-offs in females, as well as in males.This work was supported by the National Science Foundation (IOS-1021633 to C.M.D. and IOS-1601685 to C.M.D. and K.N.S.) and the Duke University Graduate School (Judy C. Woodruff Fellowship, Fred and Barbara Sutherland Fellowship and Katherine Goodman Stern Fellowship to K.N.S.). Vehicle costs in the field were supported by Duke University (research funds to C.M.D.). We relied on records of individual life histories and access to a field site maintained by the KalahariMeerkat Project (KMP). During the span of this study, the KMP was supported by the European Research Council (Research grant no. 294494 to T.H.C.-B.), the University of Cambridge, the University of Zurich, the Mammal Research Institute at the University of Pretoria and Duke University.http://rsos.royalsocietypublishing.orgam2019Mammal Research Institut

An intergenerational androgenic mechanism of female intrasexual competition in the cooperatively breeding meerkat.

Female intrasexual competition can be intense in cooperatively breeding species, with some dominant breeders (matriarchs) limiting reproduction in subordinates via aggression, eviction or infanticide. In males, such tendencies bidirectionally link to testosterone, but in females, there has been little systematic investigation of androgen-mediated behaviour within and across generations. In 22 clans of wild meerkats (Suricata suricatta), we show that matriarchs 1) express peak androgen concentrations during late gestation, 2) when displaying peak feeding competition, dominance behaviour, and evictions, and 3) relative to subordinates, produce offspring that are more aggressive in early development. Late-gestation antiandrogen treatment of matriarchs 4) specifically reduces dominance behaviour, is associated with infrequent evictions, decreases social centrality within the clan, 5) increases aggression in cohabiting subordinate dams, and 6) reduces offspring aggression. These effects implicate androgen-mediated aggression in the operation of female sexual selection, and intergenerational transmission of masculinised phenotypes in the evolution of meerkat cooperative breeding

A functional definition to distinguish ponds from lakes and wetlands

Ponds are often identified by their small size and shallow depths, but the lack of a universal evidence-based definition hampers science and weakens legal protection. Here, we compile existing pond definitions, compare ecosystem metrics (e.g., metabolism, nutrient concentrations, and gas fluxes) among ponds, wetlands, and lakes, and propose an evidence-based pond definition. Compiled definitions often mentioned surface area and depth, but were largely qualitative and variable. Government legislation rarely defined ponds, despite commonly using the term. Ponds, as defined in published studies, varied in origin and hydroperiod and were often distinct from lakes and wetlands in water chemistry. We also compared how ecosystem metrics related to three variables often seen in waterbody definitions: waterbody size, maximum depth, and emergent vegetation cover. Most ecosystem metrics (e.g., water chemistry, gas fluxes, and metabolism) exhibited nonlinear relationships with these variables, with average threshold changes at 3.7 ± 1.8 ha (median: 1.5 ha) in surface area, 5.8 ± 2.5 m (median: 5.2 m) in depth, and 13.4 ± 6.3% (median: 8.2%) emergent vegetation cover. We use this evidence and prior definitions to define ponds as waterbodies that are small (< 5 ha), shallow (< 5 m), with < 30% emergent vegetation and we highlight areas for further study near these boundaries. This definition will inform the science, policy, and management of globally abundant and ecologically significant pond ecosystems.Fil: Richardson, David C.. State University of New York at New Paltz; Estados UnidosFil: Holgerson, Meredith A.. Cornell University; Estados UnidosFil: Farragher, Matthew J.. University of Maine; Estados UnidosFil: Hoffman, Kathryn K.. No especifíca;Fil: King, Katelyn B. S.. Michigan State University; Estados UnidosFil: Alfonso, María Belén. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Bahía Blanca. Instituto Argentino de Oceanografía. Universidad Nacional del Sur. Instituto Argentino de Oceanografía; ArgentinaFil: Andersen, Mikkel R.. No especifíca;Fil: Cheruveil, Kendra Spence. Michigan State University; Estados UnidosFil: Coleman, Kristen A.. University of York; Reino UnidoFil: Farruggia, Mary Jade. University of California at Davis; Estados UnidosFil: Fernandez, Rocio Luz. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Hondula, Kelly L.. No especifíca;Fil: López Moreira Mazacotte, Gregorio A.. Leibniz - Institute of Freshwater Ecology and Inland Fisheries; AlemaniaFil: Paul, Katherine. No especifíca;Fil: Peierls, Benjamin L.. No especifíca;Fil: Rabaey, Joseph S.. University of Minnesota; Estados UnidosFil: Sadro, Steven. University of California at Davis; Estados UnidosFil: Sánchez, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Ecología, Genética y Evolución de Buenos Aires. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Ecología, Genética y Evolución de Buenos Aires; ArgentinaFil: Smyth, Robyn L.. No especifíca;Fil: Sweetman, Jon N.. State University of Pennsylvania; Estados Unido

Data from: Androgens predict parasitism in female meerkats: a new perspective on a classic trade-off

The immunocompetence handicap hypothesis posits that androgens in males can be a ‘double-edged sword’, actively promoting reproductive success, while also negatively impacting health. Because there can be both substantial androgen concentrations in females and significant androgenic variation among them, particularly in species portraying female social dominance over males or intense female–female competition, androgens might also play a role in mediating female health and fitness. We examined this hypothesis in the meerkat (Suricata suricatta), a cooperatively breeding, social carnivoran characterized by aggressively mediated female social dominance and extreme rank-related reproductive skew. Dominant females also have greater androgen concentrations and harbour greater parasite loads than their subordinate counterparts, but the relationship between concurrent androgen concentrations and parasite burdens is unknown. We found that a female's faecal androgen concentrations reliably predicted her concurrent state of endoparasitism irrespective of her social status: parasite species richness and infection by Spirurida nematodes, Oxynema suricattae, Pseudandrya suricattae and coccidia were greater with greater androgen concentrations. Based on gastrointestinal parasite burdens, females appear to experience the same trade-off in the costs and benefits of raised androgens as do the males of many species. This trade-off presumably represents a health cost of sexual selection operating in females

Additional results (associations between female status and androgens) and tables from Androgens predict parasitism in female meerkats: a new perspective on a classic trade-off

Additional results about the relationship between social and reproductive status and FAM concentrations; Tables of GLMM and GLM results for factors associated with infection status (Table S1) and abundance (Table S2