Robin Hare: Notes on a pollen-based sexual economy

In our latest blogpost, Dr. Robin Hare, Tutor at the University of Western Australia and Senior Biologist at Bennelongia Environmental Consultants, discusses with us his recently published paper in Functional Ecology: “Evolutionary divergence via sexual selection acting on females in a species with sex role reversal.”

About the paper

Our paper is about how ecology and evolution uniquely affect females in a species of bushcricket found in Western Australia. We call these bushcrickets “zaps”—a shortening of their scientific classification as ZAProchiline tettigoniid orthopterans, specifically Kawanaphila nartee. Zaps can teach us a lot about both ecology and evolution because of their mating system, which is driven entirely by the availability of food.

A mated female on a kangaroo paw, painted with red spots from an experiment (credit: Robin Hare)

Males produce large nutritive nuptial gifts comprising some 20% of the contributing male’s body weight. Males transfer this gift to females during copulation along with a packet of sperm, plugging the combined mass into the female’s reproductive tract. While the female chews through the gritty gift, sperm are transferred into her reproductive tract; once she has eaten the gift, she then eats whatever’s left of the sperm packet. Following copulation, the male will spend up to a week synthesising a new gift, and will then broadcast his readiness to mate by rubbing his vestigial wings against a small file on his back, producing a characteristic click-click in the ultrasonic range.

The rich and reliable source of nutrition provided by males is of particular interest to females early in the breeding season. Zaps eat only pollen and nectar, so are active only during spring (September to November in the southern hemisphere). Early in the breeding season, through September and much of October, there are few sources of pollen and nectar available: some grasses, peas, buttercups, and kangaroo paws—the iconic floral emblem of Western Australia.

During this period of limited floral resources, females compete with one another to reach calling males ahead of their rivals. We previously showed that ear size—a proxy for hearing sensitivity—is under selection in females. That is, females with larger ears are more successful in producing offspring than females with smaller ears. This arrangement of females competing over males is called sex-role reversal and is rare in nature.

But zaps go even further than that in their uniqueness. From mid-late October, grasstrees begin flowering, introducing massive quantities of pollen and nectar into ecosystems where they grow. When grasstrees start flowering, female zaps no longer seek out males for matings and nutritional gifts; instead, they tend to flock towards the pollen buffets provided by grasstrees and ignore males altogether. At this time, males become the competitive sex, and sex roles conform to the more common pattern seen across nature (i.e. choosy females and competitive males). In this way, zaps constitute one of the only species in the world known to undergo a predictable and quantifiable shift in sex roles within a single generation.

A female forages on a grasstree scape in Kings Park, with ear visible behind the forelimb (credit: Robin Hare)

Until this paper, there were around two dozen studies on zaps, all based on a single population living in Kings Park—a botanical garden in the heart of metropolitan Perth. The phenomenon of sex-role reversal (and subsequent de-reversal) was well known at Kings Park, but no one knew whether zaps from other populations also underwent sex-role reversal. A particularly intriguing possibility in this arena was that different floral associations in different habitats may in turn lead to different mating behaviours, and potentially even drive the evolution of new species. After all, zaps are only alive for a few months of the year, are flightless, and tend to forage in very small areas; it seemed very likely that populations hundreds of kilometres apart were not interbreeding.

This paper explored these avenues. We found that female ear size varied more than one would expect due to chance among populations of zaps found around Perth. We infer from this finding that different populations experience different durations and/or intensities of sex-role reversal, leading to differences in ear size. In Koondoola Regional Bushland, 15 km north of Kings Park, females had larger ears, and, in general, floral resources were scarce. We suggest that females at the Bushland probably undergo longer or stronger periods of sexual selection than females in other parks.

We also genotyped specimens from throughout the zaps’ natural range—from Perth in the south to Kalbarri some 600 km north. Samples from a given population were much more closely related to each other than to samples from different populations, suggesting that gene flow between populations is relatively limited. Together, these findings show that divergences among populations can certainly arise in zaps, and may be driven partly by evolutionary forces acting on females.

A female forages on a Conostylis flower in Kings Park, with ear conspicuous behind the forelimb (credit: Robin Hare)

There are many papers about how evolutionary forces acting on males cause populations diverge, but ours is one of the first papers to examine the same phenomenon among females. My PhD thesis was generally concerned with advancing the study of female animals as subjects of sexual selection; this paper contributes to that argument by showing that females do not need to be under continuous or particularly strong sexual selection for evolutionary consequences to arise.

Nevertheless, much more remains to be learned from zaps. More detailed morphological and molecular analyses of zaps, especially from Koondoola Regional Bushland, will help to unravel the causes and effects of sexual selection on female zaps. For example, what exactly is the link between ear size and hearing sensitivity? What plants do zaps eat and in what quantities, and does the diet differ between different populations? What predators, if any, predate upon zaps? Answering these and other questions help us understand both evolution and ecology.

About the research

The ecological dimension has been the greatest contribution of zap research. Zaps show us that stereotypical “male” and “female” behaviours are not innate in animals. Rather, behaviours are expressed in response to environmental stimuli. Among zaps, sex roles change with changing floral abundance: both sexes hatch ready to be competitive or to be choosy, and the prevailing ecological conditions determine which behaviour is expressed.

Presumably all animals are similarly flexible, but the ecological conditions that stimulate different behaviours do not arise. For example, considering that female mammals undergo prolonged pregnancy and lactation periods, it is difficult to imagine male contributions becoming sufficient to offset those of females, which would be necessary to tip a species into sex-role reversal (humans perhaps come closest, among the mammals). Zaps constitute a special case because the males produce such valuable gifts and females often have little other access to food early in the breeding season. As such, zaps have long been celebrated as touchstones of sexual selection research.

A female consumes a nuptial gift (credit: Robin Hare)

In addition to being scientific touchstones, however, zaps can also be difficult to find. In Kings Park, one need only approach a flowering plant on a spring evening to find zaps in abundance. In other metropolitan parks, though, zaps are more shy; still, calling males are readily detected using a bat detector tuned to 50 kHz. Further afield, zap behaviour seems to change. Males give intermittent rather than continuous calls, and tend to shelter amidst complex thickets of wiry vegetation at ground level, rather than perching conveniently on flower stems.

This behavioural crypsis made it difficult to collect sufficient numbers of zaps for the population analyses in our paper. I spent much of spring 2019 looking high and low for zaps, and even finding singletons or rare pairs in country towns like Harrismith, Eneabba, or Howatharra, but only returned with high enough numbers from Kalbarri and Cervantes. In spring 2020, I therefore pivoted to exploring Perth’s natural parks; again, I found small numbers at a variety of parks, but only found sufficient numbers in the populations reported in the paper.

I do not know why zaps are so much more abundant in Kings Park than in other places, but I have some ideas. The vegetation at Kings Park flowers in neat succession: as earlier flowers fade, new flowers are always blossoming, providing a steady stream of nutrition for the zaps as they develop from nymphs to adults. Kings Park is also relatively large, and hosts a rich diversity of native flowers. Other parks have different vegetation types, which may not be as supportive of zap populations. Additionally, while there are no gleaning bats in Kings Park, there may be bats or other predators in other parks that target zaps. The behaviour of males calling from sheltered places amidst tangled vegetation certainly seems to suggest that there are predators worth hiding from in those ecosystems. However, little is known about the ecological role of zaps, and nothing at all beyond Kings Park.

About the author

Robin in the field scouting for zap habitats in 2019. No zaps were found at this location, but thorny devils (Moloch horridus) were abundant (credit: Robin Hare)

I would say overall that this paper is my favourite of those produced during my PhD. I particularly enjoy that the colours of the figures are all derived from photographs of zaps, which come in a fascinating range from dark grey to a faint mauve, from yellow to vivid green. I am also pleased that this paper extends zap research beyond Kings Park for the first time. But I did not become involved in ecology to study zaps; I was first interested in the factors determining human mate choice. Humans are even more difficult to study than zaps, though, so after my Honours studies I pivoted to the unusual insects, and quickly became rather fond of them (they are quite disarming in person).

Beyond biology, in my spare time I write novels, play guitar, and run a YouTube channel analysing movie structure called Equipment For Living. My advice to other ecologists would be not to overlook potential study species in the proverbial backyard. Looking for zaps throughout Western Australia gave me a wonderful opportunity to explore my beautiful home state, and I found the experience greatly inspiring and rewarding.

Enjoyed the blogpost? Read the research here!

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