Polyandry and Polygyny in a Social Rodent: An Integrative Perspective Based on Social Organization, Copulations, and Genetics

John L Hoogland,Regina Trott,Stephen R Keller

doi:10.3389/fevo.2019.00003

Abstract

Animal mating systems have fascinated biologists for thousands of years. Accurate descriptions of mating systems are nonetheless elusive, because social organization can be difficult to quantify, documentation of copulations is often challenging, many copulations do not produce offspring, and genetic assignments of parentage are usually expensive. From a 7-year study of colonial white-tailed prairie dogs (Cynomys leucurus) living under natural conditions in Colorado USA, we estimated the frequencies of polyandry (i.e., copulation with >2 males) and polygyny (i.e., copulation with >2 females) from three independent approaches: (1) determination of the number of males and females living in the same territory (social organization); (2) observations of copulations; and (3) genetic assignments of paternity from seven polymorphic microsatellites. For polyandry, behavioral observations and genetics indicate similar overall percentages (27%), but social organization indicates a much lower percentage (2%). For polygyny, behavioral observations indicate the highest overall percentage (84%), then social organization (59%), then genetics (46%). All three approaches show striking annual variation in the frequencies of polyandry and polygyny. Long-term studies that integrate behavioral and genetic insights provide a detailed view of a mating system, but feasibility will depend on ease of capture, visibility of copulations, length of mating season, research objectives, genetic variation, and finances.

Highlights

Biologists have been studying mating systems for >2,300 years (Darwin, 1871; Aristotle, 1943; Trivers, 1972; Smith, 1984; Eberhard, 1996; Parker and Birkhead, 2013)
For an avian or mammalian species in which the typical pattern is for a single male and a single female to care for juveniles in an isolated nest or den, for example, a behavioral ecologist might hypothesize that females are behaviorally monandrous and males are behaviorally monogynous (Lack, 1968; Kleiman, 1977; Wittenberger and Tilson, 1980; Getz et al, 1990; Mock and Fujiok, 1990; Reichard and Boesch, 2003; Klug, 2018)
For these assessments from combined support, we evaluated the genetic evidence in two ways: (a) from the maximum likelihood of paternity (LOP) with an 80% probability threshold, and (b) from the non-exclusion of candidate males having zero allelic mismatches with the offspring being examined

Summary

Introduction

Biologists have been studying mating systems for >2,300 years (Darwin, 1871; Aristotle, 1943; Trivers, 1972; Smith, 1984; Eberhard, 1996; Parker and Birkhead, 2013). We determined combined genetic and behavioral support for paternity for three different (often overlapping) criteria for candidate males: (1) whether the male lived in the mother’s home territory, (2) whether the male was observed to copulate with the mother, and (3) whether the male could be assigned paternity from genetics.

Results

Conclusion