Part 3. Humans are (Blank) -ogamous: More on Promiscuity, & Genetics

This is the third part on the evolution of human mating behavior, comparing evidence for promiscuity and pair-bonding in our species. Please see the introduction here.


Part 2 pertained to human behaviors that suggested a human propensity for promiscuity (primate sexuality, the excessive sexual capacity of humans, infidelity rates, cultural variation in marriage practices, number of lifetime sex partners, etc.). This post and the next are concerned more with clues from our genes, anatomy, and physiology suggesting promiscuity. I realize these things are not clearly demarcated. My advisor at Binghamton, Mike Little, liked to say that “biology is behavior, and behavior is biology.” But I think in general most people would agree that while behavior has a genetic component, it is more plastic than are anatomical structures.

We left off with a list of six traits hinting at promiscuity. I don’t want to simply rehash what Ryan and Jethá address, so this post addresses some additional points on genetics before returning to their book in the next submission. Continuing with that list…

Fetal ultrasound at 4.5 months, profile view

7. Imprinted genes. Ryan and Jethá do not address genetics much, but the presence of imprinted genes in our DNA could bolster their case that promiscuity in our ancestry left behind a trail of clues in our biology. Maybe. The jury is still out on how this applies to humans. Most genes follow simple Mendelian rules, with one copy inherited from each parent and are thereafter expressed ‘biallelically’ (in pairs), with a gene’s effects being independent of whether it comes from the mother or father. But a small percentage of genes are ‘imprinted’ and expressed monoallelically, where only one copy is active, and the other copy from either mom or dad is silenced. Why would this evolve?

It appears that many imprinted genes have to do with early development, with the father’s genes directing increased placental/ fetal growth and nursing, and the mother’s copy trying to keep growth from spiraling out of control and sapping her resources and health (Sapolsky 1999). Consistent with this notion of parental conflict is that imprinted genes are found in placental and marsupial mammals, where fetal development takes place inside the mother, but have yet to be found in fish, birds, reptiles, or even in monotreme mammals like the platypus, which retained the ancestral condition of laying eggs (Renfree et al 2009). One possible reason for this is that once a fertilized egg is laid outside the body, the die is cast, and paternal genes can no longer influence the amount of nutrients directed from the mother to a growing embryo. Nor is there a need for maternal genes to counteract this. The biology behind all this is fairly complex (see Burt and Trivers 2006), but it is relevant to the current topic of promiscuity/ monogamy because:  

the “interests” of maternally derived and paternally derived alleles are identical when all costs to a mother’s (remaining reproductive potential) are associated with an equal cost to the father’s, and vice versa. This would be the case, for example, if individuals of both sexes were constrained to have all of their offspring with a single partner. Therefore, there would be no selective force favoring the origin of imprinted expression in a species with strict lifetime monogamy” (Haig 2000: 15, emphasis added).

In other words, for a perfectly monogamous mammalian species, maternal and paternal genetic interests are well aligned: offspring have half of the genes of each parent, who both wish for their current (and future) progeny to be healthy and make it to the age of reproduction. This also depends on the continued good health of each partner within a pair-bond. By comparison, in a promiscuous or serially monogamous species, the reproductive interests of both parents overlap less. Therefore, imprinted genes that better serve the interests of one parent might be favored by natural selection. In a promiscuous species, a mother’s genetic ‘strategy’ is to spread her resources among offspring from different fathers, increasing the variation in her young and the chances that at least some of them will thrive (like diversifying one’s stock portfolio). However, from the father’s vantage point, natural selection could favor genes that direct more resources to the fetal development of his own offspring, even at the cost of the health of the mother and her future reproductive prospects. (By the way, to absolve those species harboring imprinted genes, this is all done at the mechanistic level of the gene and epigenetics, not some conscious sinister plot).

This is more than theoretical. Over forty years ago, Wallace Dawson cross-bred two closely related species of mice, looking for possible reproductive barriers that could lead to speciation (Dawson, 1965). These included the sexually promiscuous deer mouse (Peromyscus maniculatus) and the more monogamous oldfield mouse (Peromyscus polionotus). The average weight outcomes of the offspring at 10 days old are seen in the table below. Offspring of true-bred deer mice and oldfield mice were about the same weight. However, offspring of promiscuous deer mouse fathers (whose genes try to augment fetal growth) and monogamous oldfield mouse mothers (without genes to counter this) were much larger. Conversely, the offspring of a promiscuous deer mouse mother – whose genes try to suppress fetal resource demands – and monogamous oldfield mouse father were much smaller. Furthermore, the runaway growth seen in the monogamous mom/promiscuous dad (oldfield X deer mouse) cross led to increased fetal and maternal mortality. Genes really can be quite selfish.

Weight at 10 days old for Peromyscus cross-matings (in grams). Data from Dawson, 1965.


Since Wallace’s study, progress has been made in describing the multiple genes involved influencing early growth in Peromyscus. The pattern is not as clear-cut as one might predict, but Burt and Trivers (2006:118) wrote that:

One interpretation of these results is that (promiscuous) P. maniculatus females silence these genes more strongly than do (monogamous) P. polionotus females, or the imprints ‘stick’ better. This difference is in the expected direction of imprinting being somewhat relaxed in the monogamous species.”

One of the best understood imprinted genes is insulin-like growth factor-2 (Igf2), which enhances fetal growth, and its receptor Igf2r. In many mammals – including mice and humans – the father’s copy of Igf2 is active in offspring while the mother’s is silenced, the effect being a tug-of-war for resources (Morison et al 2005). A different pattern is found for the receptor Igf2r. In mice, the maternal copy is active, while the father’s is not, again with the same effect. Looking across different species, Killian et al (2001) estimated that Igf2r imprinting originated roughly 150 million years ago in some mammals, but was subsequently lost 75 million years ago in the lineage leading to tree shrews, flying lemurs, and primates (including humans). Primates, of course, have a wide range of mating patterns. Therefore, knowing the imprinting status of any single gene is insufficient to reveal any species’ particular mating patterns because it could have been added/deleted at almost any point in the evolutionary past and passed down simply by legacy. A wider net must be cast, looking at different mammalian taxa.

All of this has been a long and winding lead-up to humans. What about us? The picture remains somewhat fuzzy as research moves rapidly. Luedi et al (2007) found 156 novel imprinted genes in the human genome, a higher than expected estimate. A recent review paper by Stumpf et al (2011) predicted that as more data come in, we should find more genomic imprinting in primate species from multi-male/ multi-female species (like chimpanzees and bonobos) than those from other mating systems, with the possible exception of dispersed orangutans. It would be fascinating to see how humans compare to these species, as well as monogamous gibbons and polygynous gorillas. Thus far, researchers such as Randy Jirtle at Duke University and others at the University of Otago in New Zealand have compiled online databases on this, but only for a few non-primate mammalian species.

Haig and Wharton (2003) hypothesized that Prader-Willi syndrome (PWS), a condition marked by low birth weight and feeding difficulties in infancy, followed by overeating in early childhood, could be related to genetic conflict between parental genomes. PWS is caused by the loss of some of the normally expressed paternal genes on chromosome 15 (the maternal copies being muted through imprinting). As a result, the lack of functional genes at that locus effectively leaves a fetus/infant with reduced demands on mothers for placental nourishment and breastfeeding, but this is then followed by excessive appetite after the breastfeeding years are over. Haig and Wharton speculated that the onset of increased appetite could be connected to unique human growth patterns and the timing of weaning, after which supplementary foods are introduced and are less of a drain on the mother than is breastfeeding. Furthermore, “this prediction is based on the plausible assumption that humans have not been strictly monogamous, otherwise costs to mothers would be associated with equal costs to fathers — because her offspring are his offspring — and there would be no selective force maintaining differential gene expression” (p. 323).

For now, we can say that monogamous mating could at least in theory lead to a decrease in imprinted genes in a species, as suggested by the Peromyscus mice example above. (The deer and oldfield mice are believed to have speciated about 100,000 years ago, so it could take some time). Yet, leftover from some point in our past, we still have a good number of imprinted genes embedded within us, suggesting that “reports of our monogamy are greatly exaggerated” (Sapolsky, 1999).

8. Population genetics and demography.

The mating structure of a population can leave behind other marks in the genome. If a population is monogamous, men and women will contribute equal numbers of genes to subsequent generations. One way this can be detected is by comparing recombination (‘crossing over’) in X-chromosomes and autosomal chromosomes. The biology works this way: X-chromosomes can recombine only in females since they alone have two copies, while males are XY. However, the other 22 pairs of autosomal chromosomes recombine in both sexes. Comparing those rates can give a sense of the ‘breeding ratio’ of males/ females in a population.

Labuda et al (2010) looked at genetic variation from the HapMap project, including West Africans (Yoruba), Utah residents of Western European ancestry, and East Asians (China/ Japan). They found signs of slightly skewed breeding ratios, “close to but greater than 1, suggesting some polygyny in the history of human populations” (p. 356). Using a different method, Dupanloup et al (2003)calculated breeding ratios via mutations on the Y-chromosome across 46 samples from six continents. They reported that the ratio of males contributing to the breeding population has increased over time “through a recent shift from polygyny to monogamy, which… possibly accompanied the shift from mobile to sedentary communities.” This sounds rather consistent with Ryan and Jethá’s argument that monogamy followed agriculture.

Finally, a third study utilized genetic data from six populations from the Human Genome Diversity Panel (French Basque, Biaka, Han Chinese, Mandenka, Melanesian, and San) to determine male/ female bias in a breeding population (Emery et al 2010). In a monogamous population, the number of breeding males and females are equal in a population and the number of X-chromosomes will be three-quarters (0.75) that of the autosomes, since there are three X-chromosomes and one Y within a breeding pair. Should that magic ratio of 0.75 fluctuate, it is indicative of a male or female bias in a breeding population.  Emery et al confirmed that there has been a ‘persistent female bias’ throughout most of human evolutionary history, suggesting “polygyny or higher female dispersal rates.” However, they also found a slightly different pattern after the out of Africa expansion in modern humans, indicating “continuous male-biased migration from African into non-African populations before the split of Asians and Europeans” (p. 853).

Still, genetics cannot tell us everything.  As mentioned in the previous post, sex and reproduction do not overlap perfectly. Population genetic studies can reveal that some individuals leave behind more descendants than others, but this is not the same as saying that individuals who did not leave behind descendants died celibate. Nonetheless, all of this suggests quite strongly that monogamy is not a very ancient pattern in humanity.


Part 4.  More on Promiscuity, Physiology (Here)

Part 5. Pair-Bonding

Part 6. Synthesis


Burt A, Trivers R. 2006. Genes in Conflict: The Biology of Selfish Genetic Elements. Bellknap. (Link)

Dawson WD. 1965. Fertility and size inheritance in a Peromyscus species cross. Evolution19:44-55. (Link)

Dupanloup I, Pereira L, Bertorelle G, et al. 2003. A recent shift from polygyny to monogamy in humans is suggested by the analysis of worldwide Y-chromosome diversity. Journal of Molecular Evolution 57:85-97. (Link)

Emery LS, Felsenstein J, Akey JM. 2010. Estimators of the human effective sex ratio detect sex biases on different timescales. The American Journal of Human Genetics 87: 848–56. (Link)

Haig D. 2000. The kinship theory of genomic imprinting. Annual Review of Ecology and Systematics 31: 9–32. (Link)

Haig D, Wharton R. 2003. Prader-Willi syndrome and the evolution of human childhood. American Journal of Human Biology 15: 320–9. (Link)

Killian JK, Nolan CM, Wylie AA, Li T, Vu TH, Hoffman AR, Jirtle RL. 2001. Divergent evolution in M6P/IGF2R imprinting from the Jurassic to the Quaternary. Human Molecular Genetics 10:1721-8. (Link)

Labuda D, Lefebvre JF, Nadeau P, Roy-Gagnon MH. 2010. Female-to-male breeding ratio in modern humans-an analysis based on historical recombinations. The American Journal of Human Genetics. 86:353-63. (Link)

Luedi PP, Dietrich FS, Weidman JR, Bosko JM, Jirtle RL, Hartemink AJ. 2007. Computational and experimental identification of novel human imprinted genes. Genome Research 17:1723–30. (Link)

Morison IM, Ramsay JP, Spencer HG. 2005. A census of mammalian imprinting. Trends in Genetics 21: 457-65. (Link)

Renfree MB, Hore TA, Shaw G, Graves JA, Pask AJ. 2009. Evolution of genomic imprinting: insights from marsupials and monotremes. Annual Review of Genomics and Human Genetics.10:241-62. (Link)

Ryan C, Jethá C. 2010. Sex at Dawn: The Prehistoric Origins of Modern Sexuality. Harper. (Link)

Sapolsky R. 1999. Sex and control. Discover May 1 (Link).

Stumpf RM, Martinez-Mota R, Milich KM, Righini N, Shattuck MR. 2011. Sexual conflict in primates. Evolutionary Anthropology 20:62–75. (Link)

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