Antagonism in nature: Sexual conflict

This texts deals with one form of antagonism in nature. Another text deals with interspecies conflict. Yet another one deals with fighting between members of the same species. For information about other ways in which animals in the wild suffer see our main page on the situation of animals in the wild.

Sex among animals in the wild is often antagonistic. This is because animals’ sexual interests conflict. In many species, the interests of males are different from those of females. An explanation that has been provided for this is that, in general, males prefer to maximize their number of offspring and mates, while females prefer to have fewer offspring and therefore fewer mates. This is because having offspring is generally a much bigger investment of resources for females than it is for males – it is females who undergo pregnancy or lay eggs, who provide most of the parental care, and, in mammals, who provide milk for their young. Male investment of energy and resources is much lower. Males therefore tend to adopt a reproductive strategy which focuses on maximizing their number of mates, while females tend to adopt a strategy of having fewer, higher quality mates.1 This asymmetry in interests leads to sexual conflict, in which males coerce females into mating with them, by physically forcing them to mate, harassing them until they accede, or by punishing refusals to mate.2 Sexual antagonism between males and females is so pervasive it has been likened to a “sexual arms race”,3 and is believed to have been a cause of both sexual dimorphism (physical differences between males and females in a given species) and speciation.4

 

Sexual coercion

Sexual coercion is common among animals of many species, including insects,5 fishes,6 birds,7 bottle-nosed dolphins, and primates.8 The victim usually struggles and attempts to escape and is often immobilized by the attacker. In some cases, it results in severe injury from actions like scalping (tearing the skin over the head) among aquatic birds. The rape attempts can be made individually or in groups, like the “rape flights” performed by groups of drakes.9 The risk of injury is high and the severity of the act may lead to the drowning of the assaulted animal. Below we will investigate some of the kinds of sexual coercion employed by males of different species, and the negative effects they have on female animals.

 

Mammals

The coercive methods employed by male animals vary widely, as do the kinds of injuries sustained by the female animals. Northern elephant seals are extremely polygynous and sexually dimorphic. Mature males, who can weigh up to 11 times the weight of an adult female, fight to control beaches and a harem of females. Male “courtship” behavior is direct and aggressive. If the female resists, the male will pin her to the ground with his massive bodyweight and bite the back of her neck repeatedly until she submits. This can result in severe injuries to the female, including bite wounds, broken ribs and internal bleeding. In some cases, the female will actually be killed by the male in the course of mating. Misplaced bites can cause lethal brain damage and the male’s massive weight can damage organs or cause internal hemorrhaging.10

The video below shows a male mating with a female by force. The difference in weight between them makes resistance futile.

Male sea and river otters are polygynous, and extremely aggressive towards the females they mate with. Mating usually takes place in the water, and the male bites the female’s muzzle, which often leaves scars, and sometimes holds her head under the water. This aggressive mating behavior sometimes results in the death of the female. A five year observational study of sea otter mortality found that, out of 105 dead sea otters, nose wounds due to mating trauma was the primary cause of death for two females, and a contributing factor in the deaths of nine more.11

The video below shows two river otters mating. Notice how the male bites the female and forces her head under the water.

Sexual coercion isn’t always contained within species. Sea otters have also been observed raping baby seals. 19 such incidents in Monterey Bay California between 2000 and 2002 were reported,12 including this one:

A weaned harbor seal pup was resting onshore when an untagged male sea otter approached it, grasped it with its teeth and forepaws, bit it on the nose, and flipped it over. The harbor seal moved toward the water with the sea otter following closely. Once in the water, the sea otter gripped the harbor seal’s head with its forepaws and repeatedly bit it on the nose, causing a deep laceration. The sea otter and pup rolled violently in the water for approximately 15 min, while the pup struggled to free itself from the sea otter’s grasp. Finally, the sea otter positioned itself dorsal to the pup’s smaller body while grasping it by the head and holding it underwater in a position typical of mating sea otters. As the sea otter thrust his pelvis, his penis was extruded and intromission was observed. At 105 min into the encounter, the sea otter released the pup, now dead, and began grooming.

 

Infanticide

Mammals

Infanticide is a common reproductive strategy for males in several species of mammals. Since females often don’t ovulate while lactating, it is in the reproductive interests of a male who has taken over a group of females to kill the children of the previous male in order to make the female available for mating with him. Infanticide has been observed in several species of primates including chimpanzees, orangutans and baboons,13 as well as in lions14 and mice.15 Infanticide is a very significant cause of infant mortality in some mammalian species. It is the cause of 21% of infant mortality in mountain gorillas;16 between 31% and 38% in Hanuman langurs,17 and approximately 25% in lions.18

The video below shows the new leader of a monkey troupe killing the children of the former leader. Despite having successfully driven off the old leader and taken control of the troupe, the females will not mate with him while they are still raising their children. The new leader therefore kills as many of their children as he can, in order to hasten the time when the females will mate with him and to ensure that their parental effort goes into raising his children rather than a rival’s. Note the violence of his attack on the infants, and how one mother continues to cling onto and carry her dead child in an apparent display of grief.

 

Birds

Most male birds have no external genitalia. They mate by balancing on top of the females and touching their cloacae together in a “cloacal kiss” (a cloaca is an opening found in many animals which is used for digestive, urinary and reproductive functions). This makes forced copulation difficult. There are male birds, such as ducks, that have evolved a phallus, apparently in order to facilitate forced copulation.19 This has engendered a “sexual arms race” between males and females. The male’s phallus makes it easier for him to copulate with unwilling females, thus overriding the female’s ability to choose a mate. This has led to a selection pressure for females – those who are better able to avoid forced mating are better able to choose good quality mates, and hence to increase their reproductive success. This pressure has led to increasing complexity in the vaginal morphology of some female aquatic birds. Two key anatomical innovations have evolved: dead end sacs, where the sperm from an unwanted coupling can be deposited without fertilizing her eggs, and clockwise coils, which make it easier for females to resist forced copulation with males as their phalluses spiral counterclockwise. These adaptations in turn led to the evolution of larger phalluses in males. It has been found that complex vaginal morphology co-evolved with male phallus length, which in turn co-varies with the degree of forced copulation in a species.20

These adaptations in females help them to avoid being fertilized against their will, but they don’t protect them from male aggression, and the suffering, injuries or even death that can result from their attacks. It has been estimated that 40% of all copulations in ducks are coerced. Unpaired male ducks will chase females in the air for several kilometers. When he catches her, a male grasps a female in his bill by her neck or the feathers on her back before mounting her and forcing copulation. Forced copulations can occur on land or in the water, and there can be several male ducks involved. Female ducks resist, and they can be injured or even killed during forced copulations. Group attacks in water, for example, can result in the female duck drowning.21

The video below shows a group of male ducks raping a female, first in the water, then on land. Note the violence of their attacks and how they hold her head underneath the water.

 

Invertebrates

Male seed beetles have sclerotized spines on their genitals which they use to overcome female resistance to mating, to penetrate the copulatory duct and to anchor themselves in place to prevent the female escaping.

Furthermore, these spines often injure the female, possibly in order to make her less likely to mate with other males. This is an example of “traumatic mating,” where male mating behavior that is harmful to the female improves the males’ reproductive fitness. In seed beetles (Callosobruchus maculatus), this antagonistic sexual relationship has led to a reproductive arms race in which males and females have evolved various adaptations, for example males evolving the spiked penis and females evolving a thicker lining to their reproductive tracts.22

Diving beetles of the family Dityscidae are predatory insects who live in water. Though they spend much of their time underwater, they are dependent on atmospheric oxygen. They must return to the surface every 8-15 minutes to replenish their oxygen supplies. There are several anatomical and behavioral adaptations which are plausibly explained by sexual antagonism between males and females.23 Males don’t engage in any courtship behavior, rather they simply grab passing females. The female beetles resist by swimming erratically and violently in an attempt to shake off the male beetle. Males of some species have evolved suction cup like adaptations on their front legs which help them to keep hold of resisting females. In order to force females to submit to mating, the males will shake them violently and keep them submerged under the water. During copulation, only the male has access to oxygen. Afterwards the male will guard the female for at least 6 hours to ensure that she doesn’t mate with another male during that time, thus ensuring his own paternity. During the post-copulatory guarding phase, the male keeps the female submerged, only periodically tilting her upwards above the surface so that she can replenish her oxygen supply.24

Gerridae, better known as water striders, are a family of insects that live on the surface of water. In most species of water strider female genitalia are exposed, and males mate with females by forcefully mounting them and inserting their genitalia into the females’ vulvar opening.25 Females of the species Gerris gracilicornis, however, have evolved a protective shield over their genitals, making it impossible for males to physically coerce females into mating, as mating cannot occur unless the female exposes her genitals. Instead of forcefully mating with females then, males of the Gerris gracilicornis species use intimidation in order to coerce females into mating. A male will begin by mounting a female. In the mounted position the female is at much greater risk from predators than the male, as the male is on top of the female, while the female is vulnerable to aquatic predators. The male uses this asymmetry of vulnerability to his advantage. While in a mounted position he begins tapping the water surface with his legs. This tapping produces ripples which attract predators. Because of the danger posed to the female by the approaching predators, it is in her interest to succumb to copulation as soon as possible. Once she succumbs and exposes her genitalia, the male stops tapping the water and proceeds to mate with the now compliant female.26 The video below shows this intimidation technique in practice. Note the tapping of the male and the struggles of the female as she tries to escape from both the male and the approaching predator:

Male fruit flies of the species Drosophila melanogaster use chemical substances in their seminal fluids to alter the physiology and behavior of the females with whom they mate. These substances can prolong the time it takes for the female to mate with another male, or even prevent remating altogether. They can also enhance her reproductive output. This comes at the expense of the female’s wellbeing, however, as they also reduce her longevity, inhibit her immune responses and alter her feeding behavior.27

Sexual conflict occurs even among hermaphroditic animals. Pseudobiceros hancockanus, for example, is a species of hermaphroditic flatworm. Each individual has two penises as well as ovaries, and is capable of fertilizing, or being fertilized by, another flatworm. However, as with sexually differentiated species, the partner who is fertilized incurs greater costs than the fertilizing partner. Hermaphroditic flatworms therefore engage in “penis fencing”. This is a behavior in which two flatworms struggle to fertilize the other by piercing the other’s epidermis and inserting semen, while avoiding being fertilized themselves. The inseminated partner then acts as the “mother,” incurring greater energy costs, while the inseminating partner acts as the “father,” incurring relatively little cost. In some species of flatworm, the struggle may last up to an hour.

The video below shows two hermaphroditic flatworms engaged in penis fencing:

To conclude, sexual conflict is extremely common. It is found in many species, from flatworms to ducks, from chimps to beetles. This conflict takes many forms, including physical aggression and rape, weaponized genitals and behavior modifying chemicals in sperm, and even infanticide. The harm it causes ranges in intensity, and it can include intense suffering, emotional trauma, physical injury and death.

For more information on the ways in which animals in the wild suffer see our main page on the situation of animals in the wild. For information about ways in which we can help see our main page on helping animals in the wild.


Further readings

Bonduriansky, R.; Maklakov, A.; Zajitschek, F. & Brooks, R. (2008) “Sexual selection, sexual conflict and the evolution of ageing and life span”, Functional Ecology, 22, pp. 443-453 [accessed on 14 July 2019].

Christe, P.; Keller, L. & Roulin, A. (2006) “The predation cost of being a male: Implications for sex-specific rates of ageing”, Oikos, 114, pp. 381-384.

Clinton, W. & Le Boeuf, B. (1993) “Sexual selection’s effects on male life history and the pattern of male mortality”, Ecology, 74, pp. 1884-1892.

Clutton-Brock, T. H. & Parker, G. A. (1995) “Sexual coercion in animal societies”, Animal Behaviour, 49, pp. 1345-1365.

itchkoff, S. S.; Welch, E. R., Jr.; Lochmiller, R. L.; Masters, R. E. & Starry, W. R. (2001) “Age-specific causes of mortality among male white-tailed deer support mate-competition theory”, The Journal of Wildlife Management, 65, pp. 552-559.

Liker, A. & Székely, T. (2005) “Mortality costs of sexual selection and parental care in natural populations of birds”, Evolution, 59, pp. 890-897.

Nunn, C. L.; Lindenfors, P.; Pursall, E. R. & Rolff, J. (2009) “On sexual dimorphism in immune function”, Philosophical Transactions of the Royal Society B: Biological Sciences, 364, pp. 61-69 [accessed on 25 February 2019].

Promislow, D.; Montgomerie, R. & Martin, T. E. (1994) “Sexual selection and survival in North American waterfowl”, Evolution, 48, pp. 2045-2050 [accessed on 14 February 2019].

Rankin, D. J. & Kokko, H. (2006) “Sex, death and tragedy”, Trends in Ecology & Evolution, 21, pp. 225-226.

Toïgo, C. & Gaillard, J. M. (2003) “Causes of sex‐biased adult survival in ungulates: Sexual size dimorphism, mating tactic or environment harshness?”, Oikos, 101, pp. 376-384 [accessed on 3 February 2019].


Notes

1 For an overview see Gage, M. J. G.; Parker, G. A.; Nylin, S. & Wiklund, C. (2002) “Sexual selection and speciation in mammals, butterflies and spiders”, Proceedings of the Royal Society B: Biological Sciences, 269, pp. 2309-2316 [accessed on 8 October 2019].

2 Clutton-Brock, T. H. & Parker, G. A. (1995) “Sexual coercion in animal societies”, Animal Behaviour, 49, pp. 1345-1365.

3 Dougherty, L. R.; van Lieshout, E.; McNamara, K. B.; Moschilla, J. A.; Arnqvist, G. & Simmons, L. W. (2017) “Sexual conflict and correlated evolution between male persistence and female resistance traits in the seed beetle Callosobruchus maculatus”, Proceedings of the Royal Society B: Biological Sciences, 284 [accessed on 29 July 2019].

4 See Gage, M. J. G.; Parker, G. A.; Nylin, S. & Wiklund, C. (2002) “Sexual selection and speciation in mammals, butterflies and spiders”, op. cit. Bergsten, J. & Miller, K. B. (2007) “Phylogeny of diving beetles reveals a coevolutionary arms race between the sexes”, PLOS ONE, 2 (6) [accessed on 2 September 2019]

5 Han, C. S. & Jablonski, P. G. (2010) “Male water striders attract predators to intimidate females into copulation”, Nature Communications, 1 [accessed on 4 December 2019].

6 Garner, S. R.; Bortoluzzi, R. N.; Heath, D. D. & Neff, B. D. (2010) “Sexual conflict inhibits female mate choice for major histocompatibility complex dissimilarity in Chinook salmon”, Proceedings of the Royal Society B: Biological Sciences, 277, pp. 885-894 [accessed on 27 November 2019].

7 McKinney, F. & Evarts, S. (1998) “Sexual coercion in waterfowl and other birds”, Ornithological Monographs, 49, pp. 163-195.

8 Connor, R. & Vollmer, N. (2009) “Sexual coercion in dolphin consortships: A comparison with chimpanzees”, in Muller, M. N. & Wrangham, R. W. (eds.) Sexual coercion in primates and humans: An evolutionary perspective on male aggression against females, Cambridge: Harvard University Press, pp. 218-243.

9 Bailey, R.; Seymour, N. R. & Stewart, G. (1978) “Rape behavior in blue-winged teal”, The Auk, 95, pp. 188-190.

10 Le Boeuf, L. J. & Mesnick, S. (1990) “Sexual behavior of male northern elephant seals: I. Lethal injuries to adult females”, Behaviour, 116, pp. 143-162.

11 Kreuder, C.; Miller, M. A.; Jessup, D. A.; Lowenstine, L. J.; Harris, M. D.; Carpenter, D. E.; Conrad, P. A. & Mazet, J. A. (2003) “Patterns of mortality in southern sea otters (Enhydra lutris nereis) from 1998-2001”, Journal of Wildlife Diseases, 39, pp. 495-509 [accessed on 22 October 2019].

12 Harris, H. S.; Oates, S. C.; Staedler, M. M.; Tinker, M. T.; Jessup, D. A.; Harvey, J. T. & Miller, M. A. (2010) “Lesions of juvenile harbor seals associated with forced copulation by southern sea otters”, Aquatic Mammals, 36, pp. 331-341.

13 Smuts, B. B. & Smuts, R. W. (1993) “Male aggression and sexual coercion of females in nonhuman primates and other mammals: Evidence and theoretical implications”, Advances in the Study of Behavior, 22, pp. 1-63.

14 Pusey, A. E. & Packer, C. (1994) “Infanticide in lions”, in Parmigiani, S.; vom Saal, F. S. (eds.) Infanticide and parental care, Chur: Harwood Academic Press, pp. 277-300.

15 Perrigo, G.; Bryant, W. C. & Vomsaal, F. (1990) “A unique neural timing system prevents male mice from harming their own offspring”, Animal Behaviour, 39, pp. 535-539.

16 Robbins, A. M.; Gray, M.; Basabose, A.; Uwingeli, P.; Mburanumwe, I.; Kagoda, E. & Robbins, M. M. (2013) “Impact of male infanticide on the social structure of mountain gorillas”, PLOS ONE, 8 (11) [accessed on 3 August 2019].

17 Borries, C. & Koenig, A. (2000) “Infanticide in hanuman langurs: Social organization, male migration and weaning age”, in van Schaik, C. P. & Janson, C. H. (eds.) Infanticide by males and its implications, Cambridge: Cambridge University Press.

18 Pusey, A.E. & Packer, C. (1994) “Infanticide in lions”, op. cit.

19 Brennan, P. L. R.; Prum, R. O.; McCracken, K. G.; Sorenson, M. D.; Wilson, R. E. & Birkhead, T. R. (2007) “Coevolution of male and female genital morphology in waterfowl”, PLOS ONE, 2 (5) [accessed on 30 July 2019]

20 Coker, C. R.; McKinney, F.; Hays, H.; Briggs, S. & Cheng, K. (2002) “Intromittent organ morphology and testis size in relation to mating system in waterfowl”, The Auk, 119, pp. 403-413.

21 McKinney, F.; Derrickson, S. R. & Mineau, P. (1983) “Forced copulation in waterfowl”, Behaviour, 86, pp. 250-294 [accessed on 27 September 2019].

22 Dougherty, L. R.; van Lieshout, E.; McNamara, K. B.; Moschilla, J. A.; Arnqvist, G. & Simmons, L. W. (2017) “Sexual conflict and correlated evolution between male persistence and female resistance traits in the seed beetle Callosobruchus maculatus”, op. cit.

23 Bergsten, J. & Miller, K. B. (2007) “Phylogeny of diving beetles reveals a coevolutionary arms race between the sexes”, op. cit. Miller, K. B. (2003) “The phylogeny of diving beetles (Coleoptera: Dytiscidae) and the evolution of sexual conflict”, Biological Journal of the Linnean Society, 79, pp. 359-388 [accessed on 24 October 2019].

24 Ibid.

25 Han, C. S. & Jablonski, P. G. (2009) “Female genitalia concealment promotes intimate male courtship in a water strider”, PLOS ONE, 4 (6) [accessed on 2 August 2019].

26 Han, C. S. & Jablonski, P. G. (2010) “Male water striders attract predators to intimidate females into copulation”, op. cit.

27 Mazzi, D.; Kesäniemi, J.; Hoikkala, A. & Klappert, K. (2009) “Sexual conflict over the duration of copulation in Drosophila montana: Why is longer better?”, BMC Evolutionary Biology, 9 [accessed on 2 August 2019]. Chapman, T. (2001) “Seminal fluid-mediated fitness traits in Drosophila”, Heredity, 87, pp. 511-521 [accessed on 2 December 2019].

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