Phalarope, by Ken Schneider. Click for source.
The phalarope female stands in front of a smaller male and guards him from other wandering females until he can mate. When she lays her eggs, she leaves him and finds another male to mate with.
The phalarope is one of the many animals (Gowaty, 1994) that exhibits polyandry – a mating system where one female courts many males. It suits the phalarope because of the characteristics of their mating: the mating season is short, there is a substantial predation risk in the breeding grounds, and the hatchlings can feed and take care of themselves relatively quickly, so there is no need for both parents to stay in order to ensure reproductive success.
Polyandrous species can be compared through their degree of polyandry, how many mates a female will have. The phalarope has a handful of males, while some honeybee queens will mate with over 50 drones (Moritz et al., 1995).
The fact that the female will mate with multiple males is known, and so the individual male will often try any trick to make sure it’s his sperm that fertilises the eggs. In many arthropods, this involves depositing a mating plug. Take the polyandrous bumblebee Bombus terrestris as an example. Mating typically lasts over 30 minutes by force – the male grips so tightly that removing him artificially will cause his penis to be ripped off – even though the sperm is ejaculated within the first two minutes (Duvoisin et al., 1999). Not only does the male ejaculate a lot more sperm than necessary or useful for the female (Baer, 2003), he uses the rest of the time to plug the female’s vaginal opening with a gelatinous cocktail that will dissolve away within 3 days – so while the female can mate within those three days, other males’ sperm will have trouble going through the plug. The timespan until the plug solidifies is also coincidentally the same timespan it takes the sperm to travel to the spermatheca, where it’s stored for use in fertilisation.
Types of polyandry:
Polyandry comes in various forms with self-explanatory names:
- Convenience polyandry: Instead of expending energy to resist fighting unwanted matings, the females just lay down and take it.
- Fraternal polyandry: Male brothers mate with one female.
- Genetic-benefit polyandry: In female arthropods that can store sperm, the female will mate with multiple males in order to have a diverse sperm pool, and thus more genetic diversity, to fertilise her eggs with.
- Mate-defence polyandry: As in the phalarope, where the female guards her multiple male mates.
- Maternal-benefit polyandry: In which females mate with multiple males due to benefits given by sexually-active males, usually nutrition or protection.
- Serial (sequential) polyandry: In which females form monogamous pairs with multiple males in succession.
- Simultaneous polyandry: Similar to serial polyandry, but forms the pairs at the same time.
- Sperm-replenishment polyandry: In which females mate with multiple males to refill their sperm banks (see genetic-benefit polyandry).
Evolution of polyandry:
While essential, mating is pretty risky business, especially for females: they lose energy, they are more conspicuous to predators, they may get infected by a sexually-transmitted parasite, and there may be injury involved (accidental or purposeful). In many species, the ejaculate or the mating plug contains toxic chemicals that reduce the female’s lifespan (Wigby & Chapman, 2005). So, polyandrous mating must bring about some hefty benefits in order for these to pay off.
At the individual female’s level, the benefit may come simply from not having to resist mating with males (Arnqvist & Kirkpatrick, 2005). In some species, females also get direct, material benefits from mating rituals. Males of many insects offer nutritious nuptial gifts which have been shown to increase the female’s fecundity (Arnqvist & Nilsson, 2000); and there is always the free protein earned by cannibalistic females. Males may also protect their females from predators or aggressive conspecifics (Arnqvist & Nilsson, 2000).
In cases where parental care is important, polyandry brings a distinct benefit by allowing parenthood to be split among many males, as seen in fairy wrens and other cooperative breeding birds. This is especially important in birds, where doing too many parental duties is associated with dying younger and thus missing out on reproductive cycles (Liker & Székely, 2005). However, it should also be noted that when too many males have been mated with, those males will each invest less care as there is too little benefit in caring for what is unlikely to be your offspring (Kokko & Jennions, 2008).
Polyandry also allows the female to choose who fathers the children by storing sperm, allowing her to choose “good genes”, or to keep trying to get better mates but always have a backup just in case (Watson, 1991). The benefit derived from females influencing patternity is now not believed to be so large (Hettyey et al., 2010), but it does play a supporting role. Polyandry is also a prerequisite for sperm competition, which does result in better genes getting passed on.
However, whether all the above benefits truly outweigh the substantial costs of multiple matings is not generalisable, and depends on the situation of every species. For example, Brown et al. (2004) conclusively find that in laboratory-bred Drosophila melanogaster, none of these benefits are found. Evans & Marshall (2005) found that they clearly exist in the sea urchin Heliocidaris erythrogramma. Same goes for guppies (Evans & Magurran, 2000). So, basically, it has to be studies on a species-by-species basis. Alternatively, it may not be a species-specific characteristic, but one determined by specific environmental factors, as eviudenced by the fact that even within species, levels of polyandry may differ (Ridley, 1988).
At a population genetic level, polyandry also has many benefits. It increases the genetic diversity of the offspring, rendering the population more resilient overall. This is especially important in eusocial and colonial animals, where higher genetic diversity results in less parasitic and pathogenic infections (Tooby, 1982). Polyandry is thus naturally selected for from a genetic point of view, and indirectly selected for from an ecological point of view. But whether these genetic benefits actually play a role in the ecological theatre is debatable – they’re clearly sensible from an evolutionary theory standpoint, but whether this is always relevant to mating choices isn’t clear (Maklakov & Arnqvist, 2009); see Firman & Simmons (2008) for an example where they are relevant. One must also keep in mind that examining everything from the gene’s point of view is just one possible framework, albeit a practical one (see the latter parts of my natural selection post).
Polyandry in humans:
Humans do not have a single mating system, with environment and society dictating our mating system. Biologically, we’re polygamous, but this has widely been socially and culturally subverted into monogamous pair-bonding, and socialisation can make humans mate in all imaginable ways – there are polygynous cultures, polyandrous cultures, monogamous cultures, polyamorous cultures, and in many cases, these aren’t really set – a monogamous culture/society can have polyandrous members (and vice versa in all permutations).
Beall & Goldstein (1981) describe one of the more celebrated cases of human polyandry, fraternal polyandry in Tibet. But even there, the polyandry is only done by high-status families – those who own land – and a strict hierarchy is present where the younger brothers are subordinate to the older ones. The rest of the tribe is monogamous and, from an evolutionary perspective, the members of the monogamous unions are at a distinct advantage since monogamous the males have a higher chance of passing on their genes to the next generation than the males in the polyandrous union.
The advantage of polyandry there is that it maintains the resources of the land that is owned within the family group. This is important, because Tibet isn’t really a productive landscape, and so having this closely-knit family raises the living standard – it’s more efficient than each brother getting a separate wife, and then having the land get separated into smaller estates, eventually resulting in strife.
Two other societies are recognised as polyandrous, and both are also fraternal polyandries. The Kandyans of Sri Lanka are the opposite of the Tibetans: here, it’s the poorer families that are polyandrous, with two brothers marrying the same woman. It’s the same in the Lepcha of northern India, where brothers marry the same woman. In both cases, it’s because the land is so poor that it takes more than two adults to produce enough food to sustain a family.
Arnqvist G & Kirkpatrick M. 2005. The Evolution of Infidelity in Socially Monogamous Passerines: The Strength of Direct and Indirect Selection on Extrapair Copulation Behavior in Females. The American Naturalist 165, 26-37.
Arnqvist G & Nilsson T. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60, 145-164.
Baer B. 2003. Bumblebees as model organisms to study male sexual selection in social insects. Behavioral Ecology and Sociobiology 54, 521-533.
Beall CM & Goldstein MC. 1981. Tibetan Fraternal Polyandry: A Test of Sociobiological Theory. American Anthropologist 83, 5-12.
Brown WD, Bjork A, Scneider K & Pitnick S. 2004. No evidence that polyandry benefits females in drosophila melanogaster. Evolution 58, 1242-1250.
Duvoisin N, Baer B & Schmid-Hempel P. 1999. Sperm transfer and male competition in a bumblebee. Animal Behaviour 58, 743-749.
Evans JP & Magurran AE. 2000. Multiple benefits of multiple mating in guppies. PNAS 97, 10074-10076.
Evans JP & Marshall DJ. 2005. Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin heliocidaris erythrogramma. Evolution 59, 106-112.
Firman RC & Simmons LW. 2008. Polyandry, sperm competition, and reproductive success in mice. Behavioral Ecology 19, 695-702.
Gowaty PA. 1994. Architects of sperm competition. TrEE 9, 160-162.
Hettyey A, Hegyi G, Puurtinen M, Hoi H, Török J & Penn DJ. 2010. Mate Choice for Genetic Benefits: Time to Put the Pieces Together. Ethology 116, 1-9.
Kokko H & Jennions MD. 2008. Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology 21, 919-948.
Liker A & Székely T. 2005. Mortality costs of sexual selection and parental care in natural populations of birds. Evolution 59, 890-897.
Maklakov AA & Arnqvist G. 2009. Testing for Direct and Indirect Effects of Mate Choice by Manipulating Female Choosiness. Current Biology 19, 1903-1906.
Moritz RFA, Kryger P, Koeniger G, Koeniger N, Estoup A & Tingek S. 1995. High degree of polyandry in Apis dorsata queens detected by DNA microsatellite variability. Behavioral Ecology and Sociobiology 37, 357-363.
Ridley M. 1988. Mating frequency and fecundity in insects. Biological Reviews 63, 509-549.
Tooby J. 1982. Pathogens, polymorphism, and the evolution of sex. Journal of Theoretical Biology 97, 557-576.
Watson PJ. 1991. Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigiosa (Linyphiidae). Animal Behaviour 41, 343-360.
Wigby S & Chapman T. 2005. Sex Peptide Causes Mating Costs in Female Drosophila melanogaster. Current Biology 15, 316-321.