Dung beetles and the sneaky f…er strategy

In a tunnel beneath a freshly deposited cowpat, two male Onthophagus dung beetles lock their elaborate horns for the right to mate with a female in a nearby nest chamber. But the winner of their physical contest is not assured of exclusive mating privileges.

In a side chamber lurks a third contender – a female look-alike, lacking the elaborate horns of his rivals. His strategy is very different: wait until they are strenuously engaged, then sneak in and mate with the receptive female.

But it’s the fourth player in the mating game – the female – who ultimately determines who wins the paternity stakes, according to Professor Leigh Simmons, Federation Fellow and director of the Centre for Evolutionary Biology at the University of Western Australia.

Simmons and his colleagues are investigating how different Onthophagus species and grylloid field crickets play the mating game, and how female choice drives the evolution of male morphology, and mating strategies.

Beetles and crickets are convenient, potentially informative models for other, harder-to-study species, including our own. Simmons uses Onthophagus beetles as a model because, under laboratory conditions, they can cram six generations into 12 months, they’re easy to manipulate experimentally, and their enormous diversity offers many permutations of the mating game.

Female choice imposes selection pressures that can cause males of very different species to converge on similar mating strategies – and even similar physical traits.

Simmons’ hornless Onthophagus males seem to have independently evolved their own version of a mating gambit observed in red deer on the island of Rum, off the west coast of Scotland, indecorously dubbed the ‘sneaky f…er strategy’.

A dominant stag must be constantly vigilant and ready to fight off testosterone-charged raiders intent on mating an unattended doe in his personal harem of does. Zoologists initially wondered why such contests don’t result in runaway sexual selection, creating huge, super-aggressive stags with massive antlers.

Their answer came when they observed timid stags with small racks preserving the status quo, by dashing in for a sneaky quickie with any compliant female while the dominant stag is contending with pretenders to his title.

Darwin recognised that sexual selection is a more potent force in shaping species than natural selection, but the elaboration of a male characteristic like antlers or tail features through quirky female preference is not an open-ended process. At some point, the exaggerated trait becomes a liability to the male, and natural selection reins it in.

---PB--- Naughty boys

Back to beetles: Simmons says that, where a high proportion of males adopt the SF strategy, there will be high levels of sperm competition. Species with a low proportion of sneakers probably invest more of their resources in combat, than in the sperm contest after the main event.

“Not surprisingly, when we looked at testis size relative to body mass, we found species that have a high frequency of sneaky males tend to have larger testes,” he says. “That’s true of both the sneaks and guards.

“We can explore these comparisons statistically, to see what other traits might be correlated with certain mating strategies. There are other factors out there that can influence testes size and the frequency of sneaking males – we can test predictions flowing from sperm-competition theory, but we can only establish associations.”

Simmons and his team have been doing some experimental manipulations of selection by setting up a system in which they can manipulate the mating system of a particular species.

“For example, we allow males and females to mate monogamously, or allow the males to compete to mate with individual females. After 20 generations – about five years, in beetle terms – we compare the size of the testes in the monogamous and polygamous lineages.

“We get evolutionary divergence: males from monogamous lines have smaller testes than those from polygamous lines. Then, if we arrange sperm competitions, males from polygamous lines with larger testes sire more progeny than monogamous males with small testes.”

Simmons says many researchers are studying species with alternative male mating strategies, looking for variation in sperm quantity and sperm quality. Such studies indicate that sneakers generally have higher quality sperm than guarders.

They produce more motile sperm, and despite the sneaky males being at a physical disadvantage in any contest with guarder males that limits their access to females, they tend to out-compete guarder males in terms of numbers of progeny.

“The maintenance of these tactics is an interesting issue, and there’s a lot of theory out there. We’re trying to identify mechanisms that help maintain these alternative tactics.

“Theory predicts that sneaker and guarder males should achieve equal fitness – a sneaker may get an advantage through the sperm contest by out-competing other males, while guarders achieve equal fitness by having access to more females.

“There’s not much empirical data out there, but game theory has developed broad, conceptual predictions.”

Simmons says females are not passive players. “If they don’t mate with multiple males, there’s no sperm competition. Females create competition by mating randomly and through their preferences for certain male behaviours – for example, they strongly prefer males that invest extra effort in courtship. They want the best male to father their offspring, and the tactics of being a sneak or a guard are not necessarily related to the ability to father the fittest offspring.

“Horned males might not have the best genes, so females increase their chances by allowing sneaks to copulate with them.”

---PB--- Small horns, big …

Simmons and his students have been studying a variety of Onthophagus species in which the size and number of horns varies considerably. Some have head horns, others have horns projecting from the pronotum, the body segment behind the head.

They found a developmental tradeoff between horn size and number, and sperm production at maturity. By cauterising the proliferating cells that form the horns during embryonic development, they have shown that no-horned males divert their developmental resources into growing larger testes – revealing a tradeoff in resource allocation.

“The species with more exaggerated horns tend to have much greater canalisation of the development of the testes – they’re much less susceptible to environmental perturbation, so selection pressure has somehow broken down the connection between environmental influences and testes size.”

Simmons and his students use field crickets to explore the selective pressures that favour the evolution of multiple mating in females – the behaviour that promotes sperm competition among males. Sperm competition is more than a simple game of numbers: quality is also important, for both sexes.

“We’re looking at how the fitness of offspring varies between polygamous and monogamous females, and we’re finding some evidence that females do gain fitness benefits for their offspring by mating with multiple males.”

Male genetic variation seems to be a factor in high survival rates in offspring after fertilisation, as opposed to actual success in fertilisation.

“The offspring hatch two weeks after fertilisation, and there appears to be a critical period of embryonic development when survival is determined by protein components of the male’s seminal fluid,” Simmons says.

“By mating with multiple males, the female gets a variety of proteins to maximise the viability of her embryos.

“We can’t determine in advance what constitutes male quality, but females that mate with multiple males end up with more offspring.”

Singing may be a proxy for genetic quality in male crickets, according to Simmons. “Males chirp at night, and females assess the song from a distance, and seem to be more attracted to some songs than others.

“Some US studies have linked song attractiveness to the quality of a male’s seminal fluid, so the female is able to assess the male’s suitability as a mate from his song.

Simmons says some genetic mechanism appears to link the two traits, but how it works is unclear – genetically superior males may simply have the resources to invest simultaneously in high quality sperm and high quality songs, where lesser males struggle to do both.

Those superior resources may not be exclusively genetic – the male that keeps itself well fed, and out of harm’s way, is likely to have a superior phenotype.

---PB--- Courtship songs

Simmons has been studying the courtship songs of several Australian cricket species. The males advertise their presence at night with long-distance chirping that the female can detect at a distance of five to six metres. If the female is sufficiently interested to follow the song to its source, the male switches to a quieter courtship song with a different temporal structure.

“One indication of male quality is immunocompetence – the ability to mount an effective immune response to pathogens. It confers major fitness advantages on a female’s offspring, increasing their chances of developing to reproductive maturity.

“We’re trying to determine if immune function correlates with male singing and courtship behaviour, and what song parameters appeal most to females.

“There also appears to be a link between semen quality and male immunocompetence, but we don’t yet understand the mechanisms involved. Males from cricket families [experimental lineages] that have to invest heavily in antimicrobial immunity tend to have lower semen quality, so they make fairly poor mates.

“We’re looking for patterns of genetic variation that correlate with male quality, including sperm quality. But sperm quality is also very sensitive to environmental perturbation.

“We’re looking at the contribution of male genetic variation by taking a series of males and mating each of them to three or four different females, and looking how particular traits vary between half-sib and full-sib offspring, which gives us a quantitative measure of genetic variation.”

One of Simmons’ research students, Renee Firman, recently completed her PhD study, in which she established a link between semen quality and sperm competition in a mouse model.

“Her project extended our work to vertebrate models. She found that, after 12 generations, semen quality and competitiveness diverged in different mouse lineages.

“Because the mouse genome project has been completed, we have the potential to identify genes coding for fertility factors, which may have important implications for studies of mammalian fertility.”

People learning of Simmons’ unusual interest in the mating strategies of beetles and crickets inevitably ask him to join the dots between the affairs of beetles and humans, and are politely rebuffed. “The only way to make a statement about mating strategies in humans is to study them in their own right,” he says.

That said, Simmons’ studies of human semen quality are revealing some remarkable parallels. Men viewing images depicting situations that would promote sperm competition produce ejaculates with faster-swimming sperm.

Cuckoldry has a long and ignoble history in human affairs. In The Rise and Fall of the Third Chimpanzee, Jared Diamond reports that anonymous surveys indicate that around 30 per cent of human couplings occur outside long-established pair bonds – close to the maximum frequency predicted by models of human mating behaviour, before the system descends into chaos.

Cuckoldry is not only a sneaky, but potentially fatal strategy. If Simmons is right, even in death, the incautious cuckold has a better than even chance of keeping the genes for his sneaky behaviour alive and swimming just that little bit faster in the human gene pool.