Patterns of parasitism in the cooperatively breeding meerkat: a cost of dominance for females

Smyth, Kendra; Drea, Christine M.

doi:10.1093/beheco/arv132

Cited by 28 publications

(39 citation statements)

References 93 publications

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“…Neither FAM nor social status was predictive of strongyle abundance. With the exception of weight, other potentially influential covariables [16] were unrelated to parasitism after including FAM in the models (figure 2).…”

Section: Resultsmentioning

confidence: 99%

“…Our focal subjects, from 12 clans (or groups), were 37 sexually mature female meerkats (11 dominant, 25 subordinate and 1 that achieved dominant status during the study and is represented in both social classes). Details about meerkat identification and monitoring can be found elsewhere [16].…”

Section: Materials and Methods (A) Study Site And Subjectsmentioning

confidence: 99%

“…To evenly distribute parasite eggs and oocysts (hereafter eggs) throughout each sample, we gently homogenized each sample prior to dividing it for parasitology and endocrine analyses. Details on sample collection, processing and storage are provided elsewhere (for hormone assays [17]; for parasitology [16]). …”

Section: (B) Sample Collectionmentioning

confidence: 99%

“…Although subordinate females show some degree of hormonal 'masculinization,' the dominant female has significantly greater concentrations of total androgen than does any other group member [12], which may enable her to restrict the development and reproduction of potential rivals [14,15]. Dominance status dramatically increases reproductive success, but can also incur immunosuppressive costs, as evidenced by increased parasitism [16]. Whether or not this cost is associated with raised androgen concentrations in females is unknown.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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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.

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Section: Resultsmentioning

confidence: 99%

Section: Materials and Methods (A) Study Site And Subjectsmentioning

confidence: 99%

Section: (B) Sample Collectionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2016

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“…Upon acquiring dominance, male and female meerkats experience energetic costs that could further limit their immune function: notably, males engage in energetically expensive bouts of scent marking and mate guarding [39], and females, beyond engaging in dominance assertions and aggressively targeting subordinate dams [72], are frequently pregnant [32,33,41,73]. Yet, consistent with immunocompetence in other species [74,75] and with parasitism in meerkats [23], we found no evidence that pregnancy, per se , was linked to immunosuppression. Our analysis, however, was limited to subordinate females, so we were unable to determine if relationships between immune function and pregnancy differed by social status.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2018

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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.

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Maternal Androgens in Dominant Meerkats (Suricata suricatta) Reduce Juvenile Offspring Health and Survivorship

Smyth‐Kabay,

Caruso,

Stonehill

et al. 2024

Ecology and Evolution

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In oviparous vertebrates, maternal androgens can alter offspring immune function, particularly early in development, but the potential for negative health effects of maternal androgens in mammals remains unclear. We investigated the relation between maternal androgens, particularly in late gestation, and offspring health in the meerkat (Suricata suricatta) by comparing offspring from (a) normative dominant and subordinate matrilines, whose dams naturally express high versus lower circulating androgen concentrations, respectively, and (b) normative dominant and antiandrogen‐treated dominant matrilines, whose dams' androgen function was intact versus blocked owing to experimental antagonism of the latter's androgen receptors (using Flutamide). Foetal offspring thus experienced three different endocrine environments (‘high’, ‘lower’ and ‘blocked’ androgens) late in prenatal development. We assessed parasitism, immune function, sex steroid concentrations and survivorship in these three offspring groups, both during juvenility and early adulthood. The juvenile offspring of subordinate control and dominant treated dams generally had lower intensities of parasite infections and greater immune function than did their peers from dominant control dams—patterns not found in adult offspring, or in relation to the offspring's concurrent hormone concentrations. Survivorship to adulthood was greatest in the progeny of treated dams. Descendants of dominant female meerkats—those in the ‘high’ prenatal androgen category—suffered increased parasitism and decreased immunocompetence as juveniles, as well as reduced survivorship relative to antiandrogen‐exposed peers, providing evidence in mammals that maternal androgens can negatively impact offspring health and survival. These intergenerational, androgen‐mediated, health effects represent early costs imposed by female intrasexual competition and its associated selection pressures.

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Patterns of parasitism in the cooperatively breeding meerkat: a cost of dominance for females

Cited by 28 publications

References 93 publications

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

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

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

Maternal Androgens in Dominant Meerkats (Suricata suricatta) Reduce Juvenile Offspring Health and Survivorship

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