Zaps and sex - flexible sex roles in Australian bushcrickets

For animals, sexual interactions are both vital and difficult. They are vital because, to pass one's genes on to the next generation, one must reproduce as much as possible. They are difficult because an interested party must not only find a member of the opposite sex, they must find a ready and willing member of the opposite sex.

Before animals (or even sexes) evolved, in the oceans some billion of years ago, this problem was probably solved by having two kinds of sex cell: many small, energetically cheap cells that competed with one another to fertilise a few large, energetically expensive cells. Animals brought this innovation forward and today behaviourally embody it: most males (producing sperm, the small, cheap sex cell) compete with one another for access to females, and most females (producing eggs, the large, costly sex cell) choose among the competing males.

These joint processes - competition within sexes and mate choice between sexes - constitute sexual selection, a type of natural selection. Over evolutionary time, sexual selection tends to produce conspicuous, flashy, ornamented, or competitive males (think shimmying peacock spiders and clashing rams) and choosy females (think rows of peahens lined up to watch parading peacocks).

There are rare exceptions to this common pattern. In a handful of species, males invest more energy and resources in offspring than females (male pipefishes and seahorses that brood developing young are examples). Females in these are larger, flashier, more ornamented, and more competitive than males. Such species are called sex role reversed. On the whole, animal species seem to have either conventional sex roles (competitive males, choosy females) or reversed sex roles (competitive females, choosy males), depending on the nature of reproduction in the species.

But of course, there's more to the story.

Zaps (zaprochiline tettigoniid bushcrickets of the species Kawanaphila nartee) are slow-moving, bumbling, flightless insects found in coastal areas of southern Western Australia. For many years, zaps have been studied in detail at Kings Park, a 400-hectare bushland and botanical garden in the heart of metropolitan Perth. Zaps feed only at night, eating pollen and drinking nectar from winter- and spring-flowering plants. Juveniles zaps feed on July-flowering plants like Hibbertia and the pea Daviesia. They mature in September, when they start to become sexually active. And this is when the interesting things start to happen.

In September and October, zaps mostly feed on kangaroo paws (Anigozanthos), and at this time their sex roles are reversed: the females compete for mates and the males are choosy. In late October and November, another food resource becomes available when grasstrees (Xanthorrhoea) start flowering, and zaps flock to them. And at this time, the sex roles revert to the more conventional pattern: males become competitive and females become choosy.

At the time zaps were first studied in detail, in the late 1980s, flexibly switching between sex roles was virtually unheard of. Zaps in Perth were the first animals anywhere in the world observed to behave like this. While other animal species seemed to have fairly fixed sex roles, zaps had both, and switched between them. Why?

The answer comes down to that other important factor in the life of any animal: food. In bushcrickets, and many other insects and spiders, males provide females with food during sex. The male spends days filling a nuptial gift in his abdomen. There are two parts to the gift. The smaller part, the ampulla, contains sperm. The larger part, the spermatophylax, contains protein-rich food, synthesised from the pollen the male has eaten. Altogether, the nuptial gift makes up about one fifth of the male's body weight.

A mating pair of Kawanaphila nartee. Photo: (c) Leigh Simmons

And during sex, he hands it over to the female. The ampulla is slotted into the female's reproductive opening, where sperm immediately begin swimming towards the eggs. His job done, the male leaves the female, who curls over to eat the spermatophylax. The spermatophylax is both gritty and sticky, like sandy glue (don't try this if you want to impress your partner), and it takes her over an hour to chew through it. By the time she's finished eating the spermatophylax, the ampulla will be largely empty and the female will eat that as well. Within 24 hours, 70% of the energy content of the male's nuptial gift is transferred to the female's eggs, increasing their chances of survival and successful hatching.

This is an important point because the capacity to produce offspring is ultimately limited by nutrition: across the animal kingdom, a female fed more or better food will produce more eggs than a starved female, and producing lots of offspring is the name of the game.

So back to the zaps in Kings Park. Early in spring, when kangaroo paws are flowering, females struggle to find enough pollen and nectar to produce eggs. Hungry females seek out males to secure their nuptial gifts, to help increase their egg production. If two females converge on one male, they'll fight over him, with a larger female usually winning. The males, meanwhile, spend their time assessing the females and being choosy. He may accept a female, hand over his nuptial gift and mate, or kick her off and keep looking. So when kangaroo paws are flowering, females are competitive and males are choosy - sex roles are reversed.

But when grasstrees start flowering, everything changes. Grasstrees are rich in nectar and pollen, and females can get more than enough nutrition from grasstree flowers to produce eggs. At this time, females are less dependent on the nuptial gifts, and no longer compete for males. But males now need to start competing for unmated females, which they do by calling from perches near the grasstrees. The few females who still wish to mate choose between males depending on qualities of their call. Males are now much less likely to reject females. So the females are choosy and the males competitive - the reversed sex roles have now reversed to become conventional. The natural puzzle has a straightforward solution: zap sex roles change back and forth depending on the availability of nutrition.

Grasstrees are an abundant source of food, and when flowering completely change the sex lives of zaps. Photo: (c) Robin Hare

The same forces probably apply to all animal species. Many animals may be capable of switching from male-like to female-like sexual behaviours. But for most animals, environmental conditions probably don't vary enough to overcome innate differences in the energetic costs of producing eggs as opposed to sperm.

In mammals, sex role reversal could probably never evolve, because female mammals females invest particularly heavily - they produce eggs, support the developing embryos and invest energetically in providing milk and parental care for weeks or months post-birth (this is unique in the animal kingdom). Male mammals would have to move mountains to equalise that investment (of all mammals, humans probably come closest, with the result that behavioural sex roles are relaxed in our species).

Zaps are special because the sexes have a roughly co-equal investment in reproduction (recall that 70% of the male's nuptial gift ends up in the eggs). Coupled with fluctuating availability of food, this is sufficient to swing the pendulum back and forth.

Zaps belong