Clark’s grebe (Aechmophorus clarkii) mating dance [43]
I’ve purposely added the words “in Animals” to the title as most people thinking about monogamy will think immediately of humans. Although humans are part of the animal world there is a tendency for us, as humans, to look at things through our anthropomorphic lenses. So I will do my best to discuss this with as few human references as possible. I will leave it up to the reader to draw parallels to human behavior.
Reproduction is, of course, an important part of any animal’s life history, and mating success is a driving force in evolution. The origin of sexual reproduction is still a mystery, especially why it has succeeded. Single-sex reproduction (females) can occur under certain environmental conditions and some species like Bdelloid rotifers and the parthenogenetic nematode, (Diploscapter pachys) [18] have abandoned sex millions of years ago. Sexual reproduction is still the main method for multi-celled and up animals. So, by talking about monogamy, we are talking about sexual reproduction. We need to know how animals mate, what happens afterward, and what happens to the young. [30] Monogamy is a situation where a single male and a single female mate. The male can stick around and can help raise young that are usually born helpless. This can be for a single mating season or it can be for life. When a male dies after mating naturally or by being eaten by the female or when a female dies after giving birth, this is considered monogamy. Monogamy is a category, a certain type of mating strategy within a spectrum of mating strategies. Thus it is a very loose category. Mating strategies form a vast space of possibilities of which Nature has explored only a small but still hugely varied portion. In this space run commonalities that run across all orders of life.
Male Competition
With a brief mention in Origin of the Species and then in 1871 with The Descent of Man, and Selection in Relation to Sex, Darwin introduced the second form of selection, sexual selection [3]. In it, he stated that male competition is a major driver. Species have two main strategies for how they handle young. In one they have many young and there is little or no care after birth. In some cases, the young must flee for their lives. In these situations, it is usually the female that is much larger. On the other, a smaller batch of young is cared for after birth. In this case, the female is usually smaller. Large male animals fighting has been the subject of countless National Geographic specials but this is not the only way males compete. In strict male polygamous hierarchies, smaller males and even males that look like females sneak past the big boys and into the harem to mate. In more promiscuous mating strategies, males have larger ejaculates or some of their sperm forms a plug after mating, what is called sperm competition. It has been suggested that monogamy allows lower-status males more opportunities to mate.
Female Choice
Darwin’s second driver of sexual selection is female choice. This was controversial at the time, especially in the second section of Descent of Man. Darwin framed his theory, however, in the Victorian platitudes of the time. Female mating choice drives secondary sex characteristics in males, the main example being the plumage of birds. This idea was sort of ignored with research going mainly into male competition. During the synthesis of evolutionary theory and genetics in the 1930s, an article by Julien Huxley in 1938 [38] which questioned the possibility of female choice or any female agency, shut down the debate for decades. In 1958 RA Fischer published a revised edition of The Genetical Theory of Natural Selection. In it, he outlined the theoretical possibility of female choice [39]. By the end of the 1960s, the empirical data was too overwhelming and in 1972 a paper by Trivers [5] set out a research plan and a set of questions that put female choice back in focus. This was helped, frankly, by the influx of female researchers into Biology in the ensuing decades.
The current thinking is that both males and females are active participants in reproduction, have separate and sometimes conflicting strategies, and how these play out within a particular environmental context creates the characteristics of sexual selection. [1] [4] Female choice has come a long way from driving secondary sex characteristics like fancy feathers or picking mates off a lek to cryptic mate choice (sperm choice) [28], maintaining the incest taboo, [28] and maybe driving some forms of speciation. [10] Chimpanzees form small bands with strict male hierarchies. Female chimps also form hierarchies but these are dominated by the larger, stronger males. Chimps have a promiscuous mating system with females mating repeatedly with every male in the group. Infanticide is common with males killing any unfamiliar infant. Males will often gang up on and kill a lone member of another group. Although the equivalent of rape has not been observed, males can use coercive aggression again a non-willing female. It is hard to see female choice as existing in such a situation. Chimp females are sexually active for a window of time before esterous. This may be a strategy to confuse males as to paternity thus reducing infanticide. Also, it has been confirmed that females are more choosy with partners during esterous than before. All this is still controversial with different groups of chimps producing different data, again the confounding factor of the environment. [2] [6] [7] As far as monogamy is concerned, sometimes a lone female and male will break away from the group and travel together for several days. This behavior is rare and to my knowledge, not yet fully studied. In contrast to chimps are a closely related species, Bonobos. Bonobos have a similar size difference between male and female, similar male and female hierarchies [9], and a similar promiscuous mating system as chimps. There is no infanticide and little male aggression. Sexual activity is year-round for both males and females and in females is completely decoupled from esterous. It is even extended before maturity. The dominant female hierarchy has been anthropomorphically described as a “lesbian sisterhood.” [40]
A form of choice has even been found in one-celled eukaryotes like yeast. When colonies of yeast run out of nutrients the cells turn into two types which combine into a single cell that forms an inert spore. This spore remains inert until it encounters nutrients again. These two different cell types perform a type of assortive mating with small cells finding small cells and large finding large. This seems to be the preferred combination for optimal fitness. It is a stretch to call either cell form male or female but assortive mating does exist and since neither “sex” survives fusion, this could be termed a form of monogamy. [17]
The how of sexual selection is being studied intensively and also the why. Biologists such as John Maynard Smith have modeled sexual selection as signaling between males and females., the signals being that of health and fitness. [32] In 1982, William Hamilton and Marlene Zuk postulated an arms race between parasites and hosts with sexual selection as a way of finding healthy mates. [41] Called the “Red Queen Hypothesis” after the Red Queen race in Lewis Carroll's Alice in Wonderland. [42] This is a persuasive argument that is useful but not universal. [37]
Red Queen race [45]
Male Gift Giving
In addition to male competition, male aggression, and the different forms of male mate guarding, there is another universal male activity that could be part of the evolution of monogamy. This is gift-giving. It is not unusual for males to give a protein-rich gift to a female either before or after copulation. This can also be a part of his body or even his whole body. This ranges from insects to mammals. Chimps eat mostly plants but occasionally meat. It is a common practice for male chimps to trade meat for sex. [8] In some species, the gift can be a pretty rock or a leaf or stick instead of food [29] Male bower birds build elaborate mating platforms to lure females [11] and other male birds build nests while some stick around to sit on eggs and or provision the young, or live in large family groups to help with parent’s young. [13] [35] This could be one possible path to monogamy, but there could be many others like environmental, sex ratio, or even spatial conditions. [21] [25] [22] The data is not consistent and this suggests that monogamy could have arisen multiple times due to different conditions.
Incest Taboo
The incest taboo extends across all animal orders, but not plants where selfing is common (but not universal.) Even in situations where siblings copulate there are few inbred births. Inbreeding does happen but the rate is low across all mating systems. This has been particularly surprising in cooperative mating systems where sometimes multiple generations breed together. How this works is somewhat of a mystery but it is clear that the incest taboo is maintained mostly by females.
Sensitivity to environmental factors
Acorn Woodpeckers, (Melanerpes formicivorus) live in either polyandrous (multiple males, one female) or polygynandrous (multiple males and females) breeding groups of monogamous pairs. All of these breeding systems can include one or more non-breeding helpers of both sexes. They are highly attuned to the yearly acorn crop and the timing of acorn ripening. Thus, an optimal ecology requires several species of oaks that ripen at different times. Acorn Woodpeckers make thousands of holes in dead trees called granaries and store their acorns for winter use.
In the lush oak forest near Carmel, Ca. is the Hastings Preserve which has a long-running (40+ years) study of the birds. The flocks there are 39% monogamous with an average of 4.5 birds per nest. Some nests can have as many as 15 breeders and helpers. There are 5 to 7 species of oak tree in the region. In another study area, Research Ranch in the foothills of the Huachuca Mountains in southeastern Arizona, the flocks are 100% monogamous with an average of 2.2 birds per nest (a few single helpers.) The sparse oak forest has only 1 to 3 species of oak and the flock migrates into Mexico for the winter. Another research area in central New Mexico has numbers between these two extremes. [44] So, in this species, collective breeding but not monogamy is very environmentally linked.
One question that I’ve yet to see answered is whether monogamy is a possible step towards collective breeding. [23] Central to this question is Hamilton’s Rule in the benefits of altruism times the relatedness of cooperators has to be greater than the cost of altruism:
R*B>C
In other words, individuals will help relatives before they will help strangers. [31] This is taken as doctrine among researchers in cooperative behavior although recently challenged by E. O. Wilson, an early proponent. Data supports Hamilton’s Rule in the maintenance of cooperative breeding, but if this behavior arose out of monogamy, how did monogamy arise? [24] Is not monogamy cooperative behavior? Certainly not among relatives as the incest taboo applies. [27] Acorn Woodpeckers have one of the most complex mating systems found in nature with multiple generations mating and helping in the same nest. Yet, incest is at about the same rate as anywhere else. It seems that cooperation, like mating systems themselves, has an environmental component that needs to be considered.
Monogamy
There is very little written about the evolution of monogamy, how it came about. Papers have been written about the maintenance of monogamy but few about the actual evolution, although the term “evolution” might be used in the title. This is a subtle but important difference. Thanks to genomics, it has been found that true monogamy, now termed genetic monogamy, is rare. What is common is social monogamy, where one or both partners engage in extra-pair copulation and, more importantly, not all the young belong to both parents, called extra-pair paternity (EPP.) [15] Animal intelligence is measured as brain mass divided by total body mass. Among birds, there is evidence that monogamy, and in particular social monogamy is driving increased brain size in birds. [12] Monogamy was at first thought exclusive to birds and humans but has been found in lizards, fish, and other mammals. [16] [19] Research in mammals, particularly prairie voles (Microtus ochrogaster) may shed light on a possible path to monogamy. Prairie voles are socially monogamous but two closely related species, montane voles (Microtus montanus) and meadow voles (Microtus pennsylvanicus) are promiscuous. Small differences in the regulatory region which controls the expression of the gene, oxytocin, were found in prairie voles but not in the other species. Oxytocin is linked to a neural receptor associated with social bonding. [33] [34]Neural development could be the key to the maintenance and perhaps the evolution of monogamy, at least in mammals. With multiple possible paths and myriad possible factors involved, [20][26] [36] I think it should be clear that monogamy in animals is well, complicated.
Complicated [20]
Kirkpatrick, Mark. “Sexual Selection and the Evolution of Female Choice.” Evolution 36, no. 1 (1982): 1–12. https://doi.org/10.2307/2407961.
Small, Meredith F. “Female Choice in Nonhuman Primates.” American Journal of Physical Anthropology 32, no. S10 (1989): 103–27. https://doi.org/10.1002/ajpa.1330320506.
Darwin, Charles. The Descent of Man, and Selection in Relation to Sex, London: John Murray, 1871. http://darwin-online.org.uk/content/frameset?pageseq=1&itemID=F937.1&viewtype=text.
Milam, Erika L. Looking for a Few Good Males: Female Choice in Evolutionary Biology (Animals, History, Culture), 2010. https://www.amazon.com/Looking-Few-Good-Males-Evolutionary/dp/1421404028.
Trivers, Robert L. “Parental Investment and Sexual Selection.” Alpine Publishing Company, 1972, 838.
Stumpf, R. M., and C. Boesch. “Does Promiscuous Mating Preclude Female Choice? Female Sexual Strategies in Chimpanzees (Pan Troglodytes Verus) of the Tai National Park, Cote d’Ivoire.” Behavioral Ecology and Sociobiology 57, no. 5 (March 2005): 511–24. https://doi.org/10.1007/s00265-004-0868-4.
Muller, Martin N., Melissa Emery Thompson, Sonya M. Kahlenberg, and Richard W. Wrangham. “Sexual Coercion by Male Chimpanzees Shows That Female Choice May Be More Apparent than Real.” Behavioral Ecology and Sociobiology 65, no. 5 (May 1, 2011): 921–33. https://doi.org/10.1007/s00265-010-1093-y.
Gomes, Cristina M., and Christophe Boesch. “Wild Chimpanzees Exchange Meat for Sex on a Long-Term Basis.” PLOS ONE 4, no. 4 (April 8, 2009): e5116. https://doi.org/10.1371/journal.pone.0005116.
Surbeck, Martin, Kevin E. Langergraber, Barbara Fruth, Linda Vigilant, and Gottfried Hohmann. “Male Reproductive Skew Is Higher in Bonobos than Chimpanzees.” Current Biology : CB 27, no. 13 (July 10, 2017): R640–41. https://doi.org/10.1016/j.cub.2017.05.039.
Majerus, M. E. “The Genetics and Evolution of Female Choice.” Trends in Ecology & Evolution 1, no. 1 (July 1986): 1–7. https://doi.org/10.1016/0169-5347(86)90056-X.
Madden, J. “Sex, Bowers and Brains.” Proceedings of the Royal Society of London. Series B: Biological Sciences 268, no. 1469 (April 22, 2001): 833–38. https://doi.org/10.1098/rspb.2000.1425.
West, Rhiannon J. D. “The Evolution of Large Brain Size in Birds Is Related to Social, Not Genetic, Monogamy.” Biological Journal of the Linnean Society 111, no. 3 (March 1, 2014): 668–78. https://doi.org/10.1111/bij.12193.
Wittenberger, J F, and R L Tilson. “The Evolution of Monogamy: Hypotheses and Evidence.” Annual Review of Ecology and Systematics 11, no. 1 (1980): 197–232. https://doi.org/10.1146/annurev.es.11.110180.001213.
Tumulty, James, Victor Morales, and Kyle Summers. “The Biparental Care Hypothesis for the Evolution of Monogamy: Experimental Evidence in an Amphibian.” Behavioral Ecology 25, no. 2 (March 1, 2014): 262–70. https://doi.org/10.1093/beheco/art116.
Thonhauser, Kerstin E., Michaela Thoß, Kerstin Musolf, Teresa Klaus, and Dustin J. Penn. “Multiple Paternity in Wild House Mice ( Mus Musculus Musculus ): Effects on Offspring Genetic Diversity and Body Mass.” Ecology and Evolution 4, no. 2 (January 2014): 200–209. https://doi.org/10.1002/ece3.920.
Solomon, Nancy G., and Alexander G. Ophir. “Editorial: What’s Love Got to Do With It: The Evolution of Monogamy.” Frontiers in Ecology and Evolution 8 (April 2020): 110. https://doi.org/10.3389/fevo.2020.00110.
Smith, C., A. Pomiankowski, and D. Greig. “Size and Competitive Mating Success in the Yeast Saccharomyces Cerevisiae.” Behavioral Ecology 25, no. 2 (March 1, 2014): 320–27. https://doi.org/10.1093/beheco/art117.
Schwarz, Erich M. “Evolution: A Parthenogenetic Nematode Shows How Animals Become Sexless.” Current Biology 27, no. 19 (October 9, 2017): R1064–66. https://doi.org/10.1016/j.cub.2017.08.040.
Kvarnemo, Charlotta. “Why Do Some Animals Mate with One Partner Rather than Many? A Review of Causes and Consequences of Monogamy.” Biological Reviews 93, no. 4 (2018): 1795–1812. https://doi.org/10.1111/brv.12421.
Klug, Hope. “Why Monogamy? A Review of Potential Ultimate Drivers.” Frontiers in Ecology and Evolution 6 (2018): 30. https://doi.org/10.3389/fevo.2018.00030.
Hoffmann, Sasha, Nigel C. Bennett, Bettine Jansen van Vuuren, and Heike Lutermann. “Space Use and the Evolution of Social Monogamy in Eastern Rock Sengis.” Ethology 126, no. 4 (2020): 393–402. https://doi.org/10.1111/eth.12983.
Firth, Josh A., Ella F. Cole, Christos C. Ioannou, John L. Quinn, Lucy M. Aplin, Antica Culina, Keith McMahon, and Ben C. Sheldon. “Personality Shapes Pair Bonding in a Wild Bird Social System.” Nature Ecology & Evolution 2, no. 11 (November 2018): 1696–99. https://doi.org/10.1038/s41559-018-0670-8.
Dillard, Jacqueline R., and David F. Westneat. “Disentangling the Correlated Evolution of Monogamy and Cooperation.” Trends in Ecology & Evolution 31, no. 7 (July 1, 2016): 503–13. https://doi.org/10.1016/j.tree.2016.03.009.
Peck, Joel R., and Marcus W. Feldman. “Kin Selection and the Evolution of Monogamy.” Science 240, no. 4859 (June 17, 1988): 1672–74. https://doi.org/10.1126/science.3381088.
Dobson, F. Stephen, Brittany M. Way, and Claude Baudoin. “Spatial Dynamics and the Evolution of Social Monogamy in Mammals.” Behavioral Ecology 21, no. 4 (July 1, 2010): 747–52. https://doi.org/10.1093/beheco/arq048.
Greenlaw, Jon S., and William Post. “Evolution of Monogamy in Seaside Sparrows, Ammodramus Maritimus: Tests of Hypotheses.” Animal Behaviour 33, no. 2 (May 1985): 373–83. https://doi.org/10.1016/S0003-3472(85)80061-0.
Nelson-Flower, Martha J., Philip A. R. Hockey, Colleen O’Ryan, and Amanda R. Ridley. “Inbreeding Avoidance Mechanisms: Dispersal Dynamics in Cooperatively Breeding Southern Pied Babblers.” Journal of Animal Ecology 81, no. 4 (2012): 876–83. https://doi.org/10.1111/j.1365-2656.2012.01983.x.
Bretman, Amanda, Devi Newcombe, and Tom Tregenza. “Promiscuous Females Avoid Inbreeding by Controlling Sperm Storage.” Molecular Ecology 18, no. 16 (August 2009): 3340–45. https://doi.org/10.1111/j.1365-294X.2009.04301.x.
LeBas, Natasha R., Leon R. Hockham, and Michael G. Ritchie. “Sexual Selection in the Gift-Giving Dance Fly, Rhamphomyia Sulcata, Favors Small Males Carrying Small Gifts.” Evolution 58, no. 8 (2004): 1763–72. https://doi.org/10.1111/j.0014-3820.2004.tb00459.x.
Lindsay, Willow R., Staffan Andersson, Badreddine Bererhi, Jacob Höglund, Arild Johnsen, Charlotta Kvarnemo, Erica H. Leder, et al. “Endless Forms of Sexual Selection.” PeerJ 7 (November 5, 2019): e7988. https://doi.org/10.7717/peerj.7988.
Møller, Anders Pape. “Parasites and Sexual Selection: Current Status of the Hamilton and Zuk Hypothesis.” Journal of Evolutionary Biology 3, no. 5–6 (1990): 319–28. https://doi.org/10.1046/j.1420-9101.1990.3050319.x.
Smith, J. M. “Theories of Sexual Selection.” Trends in Ecology & Evolution 6, no. 5 (May 1991): 146–51. https://doi.org/10.1016/0169-5347(91)90055-3.
Lieberwirth, Claudia, and Zuoxin Wang. “The Neurobiology of Pair Bond Formation, Bond Disruption, and Social Buffering.” Current Opinion in Neurobiology 40 (October 2016): 8–13. https://doi.org/10.1016/j.conb.2016.05.006.
Young, Larry, and Zuoxin Wang. “The Neurobiology of Pair Bonding.” Nature Neuroscience 7 (November 1, 2004): 1048–54. https://doi.org/10.1038/nn1327.
Brotherton, NM, and A Rhodes. “Monogamy without Biparental Care in a Dwarf Antelope.” Proceedings of the Royal Society of London. Series B: Biological Sciences 263, no. 1366 (1996): 23–29.
Culina, Antica. “Trading up: The Fitness Consequences of Divorce in Monogamous Birds.” Biological Reviews, 2015. https://onlinelibrary.wiley.com/doi/10.1111/brv.12143.
Møller, Anders Pape. “Parasites and Sexual Selection: Current Status of the Hamilton and Zuk Hypothesis.” Journal of Evolutionary Biology 3, no. 5–6 (1990): 319–28. https://doi.org/10.1046/j.1420-9101.1990.3050319.x.
Huxley, Julian S. “The Present Standing of the Theory of Sexual Selection.” Evolution: Essays on Aspects of Evolutionary Biology, 1938, 11–42.
Fischer, RA. “The Genetical Theory of Natural Selection (Revised and Enlarged Version of the Work, Originally Published 1930).” Dover Publ., New York, 1958.
Clay, Zanna, and Klaus Zuberbühler. “Communication during Sex among Female Bonobos: Effects of Dominance, Solicitation and Audience.” Accessed December 3, 2021. https://core.ac.uk/reader/8688960.
Hanilton, William, and Marlene Zuk. “Heritable True Fitness and Bright Birds: A Role for Parasites?” Science, 1982. https://www.science.org/doi/abs/10.1126/science.7123238.
Lewis, Carroll. “Alice’s Adventures in Wonderland,” 1865. https://www.gutenberg.org/files/11/11-h/11-h.htm.
The Spruce. “Bird Mating Dances and Other Courtship Behavior.” Accessed December 17, 2021. https://www.thespruce.com/bird-courtship-behavior-386714.
Koenig, Walter, Eric L Walters, and Joseph Haydock. “Acorn Woodpeckers, Helping at the Nest, Polygynandry, and Dependence or a Variable Acorn Crop.” In Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution, and Behavior, edited by Walter D. Koenig and Janis L. Dickinson. Cambridge: Cambridge University Press, 2016. https://doi.org/10.1017/CBO9781107338357.
By John Tenniel - Алиса в зазеркалье. Оригинальные гравюры Джона Тенниела, Public Domain, https://commons.wikimedia.org/w/index.php?curid=14629431
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