Genetic Monogamy in Socially Monogamous Mammals Is Primarily Predicted by Multiple Life History Factors: A Meta-Analysis

Abstract

Background: We still do not understand the key drivers or prevalence of genetic monogamy in mammals despite the amount of attention that the evolution of mammalian monogamy has received. There have been numerous reviews of the hypotheses proposed to explain monogamy, some of which focused on animals in general, while others focused on particular classes like birds or mammals, or on specific orders within a class. Because monogamy is rare in mammals overall but relatively common in some of the orders in which it has been observed (e.g., Primates, Macroscelidea, and Carnivora), mammals provide a unique taxon in which to study the evolution and maintenance of monogamy However, the term "monogamy" encompasses related but separate phenomena; i.e., social monogamy (pair-living by opposite-sex conspecifics) and genetic monogamy or reproductive monogamy (mating exclusivity). A recent review of mammalian monogamy reported that 226 species (9%) in 9 orders (35%) were socially monogamous, although socially monogamous mammals are not necessarily genetically monogamous.Methods: Since factors that predispose socially monogamous mammals to be genetically monogamous are still subject to debate, we conducted meta-analyses using model selection to determine the relative importance of several life history, demographic, and environmental factors in predicting genetic monogamy. Results:We found sufficient data to include 41 species in our analysis, about 2x more than have been included in previous analyses of mammalian genetic monogamy. We found that living as part of a socially monogamous pair vs. in a group was the best predictor of genetic monogamy, either by itself or in combination with high levels of paternal care. A male-biased sex ratio and low population density were inversely related to the number of pairs that were genetically monogamous, but not to the production of intra-pair young or litters. Conclusion:Our results agree with the results of some previous analyses but suggest that more than one factor may be important in driving genetic monogamy in mammals.

Mate choice, reproductive success and inbreeding in white rhinoceros: New insights for conservation management

“…Monogamy is infrequent in mammals and usually occurs in socially monogamous species such as in primates or rodents (Lambert, Sabol, & Solomon, 2018;Ophir, Phelps, Sorin, & Wolff, 2008).…”

Monogamy: Cause, Consequence, or Corollary of Success in Wild Canids?

“…Female choice likely contributed to the evolution of paternal care (Kvarnemo, 2005;Lukas and Clutton-Brock, 2013;Lambert et al, 2018). Kvarnemo (2005) suggested that if females select males that care for young, this can explain the correlation often observed between paternity and male care but in the opposite direction of causation to that often suggested (i.e., caring males are more likely to sire offspring, rather than males that sire offspring are more likely to provide care).…”

“…Furthermore, even with large litters, a female can compensate for the male's work when he is absent or reduces investment (although at apparent cost to her health and survival, therefore compromising potential future reproductive success) (Sacks and Neale, 2001;Cameron et al, 2011) and females may adjust effort according to litter size (Mech et al, 1999), supporting that male care can be a female preference, rather than pure necessity. Lambert et al (2018) suggested that monogamy and paternal care co-evolved when selection initially favored affiliative males, which subsequently evolved into paternal care.…”

“…Social monogamy is no guarantee of genetic monogamy, i.e., exclusive mating (Klug, 2018;Lambert et al, 2018), and, indeed, almost every genetically studied canid species has revealed extrapair paternities (EPP) (see Hennessy, 2007 for an exception). For example, extra-pair males sired 25% of 16 offspring in Island foxes (Roemer et al, 2001), 52% of 19 offspring from 15 litters in swift foxes , 31% of 176 offspring in arctic foxes (Cameron et al, 2011) and in red foxes from 38% of 38 offspring (Iossa et al, 2008b) to as much as 80% of 30 offspring .…”

“…Monogamy has long been an area of interest for evolutionary and behavioral ecologists (Orians, 1969;Emlen and Oring, 1977) and numerous early hypotheses attempted to explain its evolution and maintenance (e.g., Orians, 1969;Emlen and Oring, 1977;Wittenberger and Tilson, 1980). Decades of empirical and theoretical research suggest factors affecting monogamy's origin and maintenance can be complex, differ among taxa, and are subject of a constant evolutionary interplay between monogamy and associated traits (Klug, 2018;Lambert et al, 2018). However, most research on monogamy has focused on birds (Reichard and Boesch, 2003), unsurprisingly since ∼90% of bird species exhibit social monogamy.…”