Low rank and primiparity increase fecal glucocorticoid metabolites across gestation in wild geladas

Sofia C Carrera; Sharmi Sen; Michael Heistermann; Amy Lu; Jacinta C Beehner

doi:10.1016/j.ygcen.2020.113494

Low rank and primiparity increase fecal glucocorticoid metabolites across gestation in wild geladas

Gen Comp Endocrinol. 2020 Jul 1:293:113494. doi: 10.1016/j.ygcen.2020.113494. Epub 2020 Apr 22.

Authors

Sofia C Carrera¹, Sharmi Sen², Michael Heistermann³, Amy Lu⁴, Jacinta C Beehner⁵

Affiliations

¹ Department of Psychology, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: scarrera@umich.edu.
² Department of Anthropology, University of Michigan, Ann Arbor, MI 48109, USA.
³ Endocrinology Laboratory, German Primate Center, Leibniz Institute for Primate Research, 37077 Göttingen, Germany.
⁴ Department of Anthropology, SUNY Stony Brook, Stony Brook, NY 11794, USA.
⁵ Department of Psychology, University of Michigan, Ann Arbor, MI 48109, USA; Department of Anthropology, University of Michigan, Ann Arbor, MI 48109, USA.

PMID: 32333913
DOI: 10.1016/j.ygcen.2020.113494

Abstract

Integrative behavioral ecology requires accurate and non-invasive measures of hormone mediators for the study of wild animal populations. Biologically sensitive assay systems for the measurement of hormones and their metabolites need to be validated for the species and sample medium (e.g. urine, feces, saliva) of interest. Where more than one assay is available for hormone (metabolite) measurement, antibody selection is useful in identifying the assay that tracks changes in an individuaĺs endocrine activity best, i.e., the most biologically sensitive assay. This is particularly important when measuring how glucocorticoids (GCs) respond to the subtle, additive effects of acute stressors during a predictable metabolic challenge, such as gestation. Here, we validate a group-specific enzyme immunoassay, measuring immunoreactive 11β-hydroxyetiocholanolone, for use in a wild primate, geladas (Theropithecus gelada). This group-specific assay produced values correlated with those from a previously validated double-antibody, corticosterone ¹²⁵I radioimmunoassay. However, the results with the group-specific assay showed a stronger response to an ACTH challenge and identified greater variation in gelada immunoreactive fecal glucocorticoid metabolites (iGCMs) compared with the corticosterone assay, indicating a higher biological sensitivity for assessing adrenocortical activity. We then used the group-specific assay to: (1) determine the normative pattern of iGCM levels across gelada gestation, and (2) identify the ecological, social, and individual factors that influence GC output for pregnant females. Using a general additive mixed model, we found that higher iGCM levels were associated with low rank (compared to high rank) and first time mothers (compared to multiparous mothers). This study highlights the importance of assay selection and the efficacy of group-specific assays for hormonal research in non-invasively collected samples. Additionally, in geladas, our results identify some of the factors that increase GC output over and above the already-elevated GC concentrations associated with gestation. In the burgeoning field of maternal stress, these factors can be examined to identify the effects that GC elevations may have on offspring development.

Keywords: Cercopithecine; Corticosterone; Cortisol; Pregnancy; Primate; Validation.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Animals, Wild / metabolism
Corticosterone / metabolism
Feces / chemistry*
Female
Glucocorticoids / metabolism*
Immunoenzyme Techniques
Male
Metabolome*
Models, Biological
Parity*
Pregnancy
Radioimmunoassay
Reproducibility of Results
Theropithecus / metabolism*

Substances

Glucocorticoids
Corticosterone