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Prolactin Receptor Gene Diversity in Azara’s Owl Monkeys (Aotus azarai) and Humans (Homo sapiens) Suggests a Non-Neutral Evolutionary History among Primates

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Abstract

Although paternal care is rare in mammals, males of several primate taxa exhibit high degrees of this behavior. Studies a number of vertebrate species found a positive correlation between prolactin (PRL) levels and paternal care. Studies of maternal care in knockout mice also indicate that the prolactin receptor (PRLR) plays a critical role in the neural regulation of parental care. To better understand the extent of PRLR genetic variation within primates, we characterized intraspecific coding variation in Azara’s owl monkeys (Aotus azarai) from northern Argentina, a species with intensive paternal care. We then examined PRLR variation in 1088 humans (Homo sapiens) from the 1000 Genomes Project. Lastly, we assessed interspecific variation in PRLR in 4 different Aotus spp. and 12 phylogenetically (and behaviorally) disparate primate taxa. Our analyses revealed that the coding region of PRLR exhibits significant variation in all species of primates, with nonsynonymous amino acid substitutions being enriched in the intracellular domain, a region responsible for activation of downstream targets in the PRL pathway. In addition, several species exhibit entire codon deletions in this region. These results suggest a non-neutral evolutionary history of the PRLR locus within different primate lineages, and further imply that the translated PRLR protein has undergone considerable change throughout primate evolution. Such changes may be driven by selection for different behaviors and physiologies resulting from modulations of the pleiotropic prolactin pathway. Yet, the genetic variants in PRLR among primate taxa do not discretely cluster with species-level differences in paternal care behaviors. These observations imply that other mechanisms must be involved in the regulation of paternal care in primates.

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Acknowledgments

The authors sincerely thank the editors and guest editors of the International Journal of Primatology for the opportunity to contribute research to this Special Issue. This study was made possible thanks to a University Research Fund award from the University of Pennsylvania (E. Fernandez-Duque), and research funds from the Department of Anthropology at the University of Pennsylvania (P. L. Babb). The authors thank the students, volunteers, and researchers who assisted with the capturing and sampling of the monkeys that led to the collection of samples used in this genetic study. Special gratitude is owed to Marcelo Rotundo for his assistance in the field during the past decade. We also thank Mr. John Adams, Mr. F. Middleton, and Ing. C. Cimino for their continuing support at Estancia Guaycolec. The Ministerio de la Producción, Subsecretaría de Ecología and Recursos Naturales from Formosa Province, the Dirección de Fauna Silvestre de la Nación Argentina, and the University of Pennsylvania IACUC board authorized and sponsored the owl monkey field research. P. L. Babb offers his thanks to the University of Pennsylvania’s Department of Anthropology and Graduate Group for project support. A. M. McIntosh thanks the Haverford College Department of Molecular Biology and Dr. Karl Johnson for their support. E. Fernandez-Duque gratefully acknowledges continuing financial support from the Wenner-Gren Foundation, the Leakey Foundation, the National Geographic Society, the National Science Foundation (BCS-0621020), and the Zoological Society of San Diego. T. G. Schurr further acknowledges the infrastructural support provided by the National Geographic Society. The authors also gratefully acknowledge the two anonymous reviewers whose thoughtful suggestions helped to strengthen this article.

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  1. Paul L. Babb

    Present address: Department of Pharmacology, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA, 19104, USA

Authors and Affiliations

  1. Department of Anthropology, University of Pennsylvania, Philadelphia, PA, 19104, USA

    Paul L. Babb, Eduardo Fernandez-Duque & Theodore G. Schurr

  2. Department of Anthropology, Yale University, New Haven, CT, 06511, USA

    Annick M. McIntosh

  3. CECOAL-Conicet, Corrientes, 3400, Argentina

    Eduardo Fernandez-Duque

Authors
  1. Paul L. Babb
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  2. Annick M. McIntosh
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  3. Eduardo Fernandez-Duque
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  4. Theodore G. Schurr
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Correspondence to Paul L. Babb.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1

Marginal density plots depicting age values (time to most recent common ancestor [tmrca]) used as priors for different clades of taxa in BEAST coalescent analysis of PRLR locus. (JPEG 84 kb)

Online Resource 2

BEAST Priors. Data Sources: a Setoguchi and Rosenberger 1987; b Hartwig and Meldrum 2002; c Tejedor et al. 2006; d Takai et al. 2000, e Beard and Wang 2004, f Simons et al. 1987, g Miller and Simons 1997. (DOCX 32 kb)

Online Resource 3

PRLR coding variation in humans and owl monkeys as depicted by MAF plotted for all polymorphic sites along the assembled 1866 bp mRNA for given data sets. Data Source: 1000 Genomes Project Consortium 2010, 2012: ftp://ftp-trace.ncbi.nih.gov/1000genomes/ftp/. (JPEG 161 kb)

Online Resource 4

Non-synonymous amino acid substitutions differentiating PRLR mRNA of humans and owl monkeys (DOCX 39 kb)

Online Resource 5

Genetic variation throughout the 200 kb region surrounding PRLR in humans. Depicted by MAF plotted for all 2980 polymorphic sites in the window of analysis. Data Source: 1000 Genomes Project Consortium 2010, 2012: ftp://ftp-trace.ncbi.nih.gov/1000genomes/ftp/. (JPEG 276 kb)

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Babb, P.L., McIntosh, A.M., Fernandez-Duque, E. et al. Prolactin Receptor Gene Diversity in Azara’s Owl Monkeys (Aotus azarai) and Humans (Homo sapiens) Suggests a Non-Neutral Evolutionary History among Primates. Int J Primatol 35, 129–155 (2014). https://doi.org/10.1007/s10764-013-9721-9

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  • DOI: https://doi.org/10.1007/s10764-013-9721-9

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