Category Archives: Condition-dependence

New paper: Food supply – not ‘live fast, die young’ mentality – makes male crickets chirpy

I have a new paper out in the journal Functional Ecology, entitled ‘Mating opportunities and energetic constraints drive variation in age-dependent sexual signalling‘. This is work from my PhD with Luc Bussière at Stirling, along with collaborators from the University of Exeter’s Cornwall campus (where I’m currently based).

We used dietary manipulations as well as manipulation of potential mate availability to investigate how male sexual signalling changes with current budget and previous expenditure. We found some cool results about what causes variation in age-dependent sexual signalling – these have implications for ‘honesty’ in sexual displays, and are also a nice reminder that there are simpler explanations than we (as humans, who love seeing patterns in the noise) often cling to.

Our paper also includes a nice example of using ‘zero-altered’ statistical models, enabling us to partition out effects on why males call from the effects on how long they call.

You can find the paper here, or email me for a PDF if you don’t have access to the journal.

Alternatively, the press office at Exeter put together a nice press release, which I’ve pasted below:


Shedding a few pounds might be a good strategy in the human dating game, but for crickets the opposite is true.

Well-fed male crickets make more noise and mate with more females than their hungry counterparts, according to research by the universities of Exeter and Stirling.

It has long been believed that males who acquire ample food can adopt a “live fast, die young” strategy – burning energy by calling to attract females as soon as they are able, at the expense of longevity – while rivals with poorer resource budgets take a “slow and steady” approach, enabling them to save resources and take advantage of their savings later in the season.

But the researchers found that increased diet – rather than any strategic decision by the cricket – led the best-provisioned crickets to chirp for longer. This had no noticeable cost to their lifespan.

Meanwhile hungrier males not only signalled less – meaning fewer female visitors – but also died younger.

Senior author Dr Luc Bussière, of the University of Stirling, said the findings offered a “simpler alternative” to understanding the behaviour of crickets.

“While it was intriguing to think that males might foresee and plan for their future reproductive prospects by strategically staying quiet, what our experiment suggests is actually easier to understand: rather than relying on an ability to forecast the future, crickets appear instead to respond mainly to the resources they have in hand,” he said.

Male crickets signal to females using an energetically expensive call, produced by rubbing together their hardened forewings.

The more time they spend calling, the more mates they attract.

The paper, published in Functional Ecology, studied decorated crickets, which mate about once a day on average during their month-long adult life.

Males need a three-hour recovery period following each mating to build a new sperm package, after which they are able to call again in the hopes of attracting another female.

Researchers found that a male cricket’s decision about whether to call was primarily based on whether females were nearby – rather than how well-fed they were – but the better-nourished males were able to call for longer and thus increase their mating prospects.

The study also provides insights into how energy budgets keep male displays honest for choosy females over the course of the mating season.

“In nature, a ‘better quality’ male will likely have better access to resources,” said lead author Dr Tom Houslay, a Postdoctoral Research Associate at the University of Exeter.

“Low-quality males might be able to ‘cheat’ by calling a lot one day, making females think they are high-quality, but this is not sustainable – so there is ‘honesty on average’.

“A female may be fooled once or twice, but over time males with more energy will call more – meaning females should tend to make the ‘correct’ decision by preferring those males.”


#ESEB2013: my poster (with all-new title and abstract…!)

I’ve just uploaded my poster to the ESEB website, so I thought I’d share it on here as well. In what I hope isn’t a flaw confined solely to myself, the title and abstract are now a little different from what I submitted way back when at the registration stage…! In fact, I ended up chucking out a lot of what I originally had on the poster, so it’s even more different now. I’ll try to put the bonus figures on here later if I get a chance. For now, I’ve put the abstract underneath the image of my poster below, in case anyone’s interested.

Click on the poster to have a look at the PDF, or alternatively just accost me in Lisbon – I’m particularly keen to talk to anyone who might be able to help me work out how to apply van de Pol and Verhulst’s work on age-dependent traits to my data, or who wants to discuss problems of age-dependent behavioural traits (and preferences?!), and also anyone who thinks they might want to employ me once I finish my PhD (well, it’s worth a shot, right?).

I’ll be hanging around my poster in the ‘Phenotypic plasticity’ symposium on Tuesday’s poster session, and otherwise will be around, being excited about all the awesome science, and more than happy to chat to anyone about insect sex, going to Borneo, or even…


You can leave your ‘too much text!’ comments at home, though. I already know.

Does phenotypic plasticity undermine the reliability of sexual advertisement or help sustain adaptive mate choice?

Exaggerated sexual traits can provide information to females about male performance, even if the precise alleles that confer high performance change along with environmental conditions. This plasticity in signalling may help to preserve genetic variation that would otherwise be eroded by strong mate choice, but it can also compromise signal reliability if environmental conditions change during development. We manipulated resource acquisition by altering the diet quality of inbred lines of decorated crickets (Gryllodes sigillatus) at both juvenile and adult stages. This allowed us to study both the effect of diet quality and a change in environment during development on trait expression. We measured a number of sexually and naturally selected traits in both sexes, revealing striking differences across diets in the expression of morphological and behavioural traits. We then assessed the reliability with which various traits signalled resource acquisition by assessing their genetic variance, as well as the covariance between traits and across environments. Our results show that traits such as body weight and calling effort, the male sexual advertisement trait, are more sensitive to environmental effects than morphological traits that are fixed at eclosion. We also show that there are high genetic correlations between the expression of lifetime calling effort in different environments. Females assess males based on current advertisement levels, rather than on a lifetime total; as an individual’s condition will mediate investment in current and future advertisement, age-dependent changes in condition can further obscure the relationship between genotype and phenotype. Genetic correlations between single measures of calling effort across environments for different age groups, and across age groups within environments, were low and even changed sign between timepoints. Variation in calling effort caused by age and environmental heterogeneity should help maintain genetic variation in sexually-selected signals, but plasticity in such complex, behavioural trait presents problems for their origin and persistence under models of good-genes mate choice.

#Evol2012: Evolution 2012 review, special Doug Emlen edition

I’m going to skip ahead in my review of the talks which I enjoyed at Evolution 2012 in Ottawa, as Doug Emlen‘s latest research has just been published in the latest issue of the prestigious journal Science. This gives me an excuse to write about his talk and the new paper, as well as to engage in gratuitous posting of beetle photos.

It makes me a bit sick when I think about how awesome this lab is.

I have a real soft spot for research on beetle horns, as followers of Nature!Sex!TopTips! may be aware, so I was really excited to see Emlen’s talk – even more so after the taster that was Erin McCullough’s presentation earlier in the week (McCullough is a PhD student co-supervised by Emlen and Bret Tobalske at the University of Montana’s ‘Flight Lab’). Research into animal weaponry often goes hand-in-hand with studies of ornaments because there is direct sexual selection upon them; females use ornaments as a basis on which to select a mate, while weapons are used by males to defeat rivals (or to assess their condition and status) and so gain access to females. Together, these exaggerated, elaborate structures are some of the most incredible sights we see in nature.

The rhinoceros beetle Trypoxylus dichotomus, used in both Erin McCullough’s work on how horn size affects flight and Doug Emlen’s research into the mechanistic basis of exaggerated trait expression. Photo copyright flickr user Mushimizu (note: open the link from this image in a new window to see the animated gif in action!)

It’s no surprise that a lot of research investigates these amazing traits, but there are still some big questions to grapple with. For example, they seem to be very reliable indicators of male quality – why should this be so? Can’t some males ‘cheat’ by somehow investing more into ornament or weapon growth than other things? Also, if females select upon a particular heritable trait, then shouldn’t we see very little variation by now, with all males having pretty much the same size of trait? Consider the range of deer antler size in comparison to, say, the range of deer leg length. Antlers are much, much more variable – but why?

Brief non-beetle interlude: red deer, showing the variability in antler size and shape. Image copyright David J Slater.

I’ve written about the maintenance of genetic variation in such traits before, both here and over at the Nothing in Biology Makes Sense blog, using the ‘genic capture’ model proposed by Rowe and Houle. This model posits that the continued evolution of sexually selected ornaments and weapons is enabled by these traits ‘capturing’ the underlying condition of the animals. An individual’s condition is affected by its general health, nutrition, parasite resistance, competitive ability, etc…  essentially, the genetic variation among males in terms of all these factors underlies the variation in these amazing traits. It’s this ‘condition-dependence’ of traits, a close association with the individual’s condition, which means that the expression level should be ‘unfakeable’ and thus a reliable indicator of male quality. Not only this, but it also allows the evolution of ever-more exaggerated ornaments and armaments. So, these traits have some particular characteristics which have triggered huge interest from an evolutionary point of view: extreme size, heightened sensitivity to condition, and much more variability than we see in other morphological traits. We often think of condition-dependence as a kind of ‘black box’ – environmental and genetic factors go in, and traits come out. Emlen’s current research asks the question of, well, what mechanism enables this to happen? What’s inside the black box that creates these incredible, extreme biological structures?

Emlen proposes that there is a developmental explanation for this, and it lies within the insulin / insulin-like growth factor (IGF) pathway. This pathway has emerged as the central mechanism in animals for integrating physiological condition with growth; insulin and IGFs not only regulate tissue growth and body size, but they are also sensitive to factors such as nutrition, stress and infection. The levels of insulin / IGF circulating in an individual would cause a graded response via this particular pathway, with growth speeding up or slowing down in response to changes in nutritional or physiological state – i.e., the same kind of factors which affect what we term ‘condition’. So far, so straightforward, you might think: there’s a pathway which controls tissue growth that depends on how healthy and well-nourished you are. But how might this lead to the evolution of highly exaggerated weapons and ornaments?

Well, here comes the even cooler bit: traits differ in how they respond to these signals. This can have a truly profound effect on the amount and nature of their growth. Some traits, like Drosophila genitalia size, are not particularly sensitive to insulin / IGF signalling, meaning that they tend to be around the same size in all individuals, no matter their nutritional state. Wings, meanwhile, are more sensitive to these signals. Within a variable population of fruit flies, with a normal range of body sizes, we would see variation in wing size approximately equal to variation in body size, while genitalia size would hardly vary at all. So, just as wings are more sensitive to insulin signalling in Drosophila than are genitals, Emlen predicted that exaggerated weapons or ornaments are even more sensitive than that. Such heightened sensitivity to insulin / IGF levels would explain how such traits grow to extreme sizes, why there is such huge variation within populations, and why such traits seem to be reliable indicators of underlying quality.

Normal beetle service has resumed: the male rhinoceros beetle Trypoxylus dichotomus. Image copyright flickr user golbenge.

Emlen and his colleagues tested this hypothesis in male rhinoceros beetles (Trypoxylus dichotomus), which have a large forked horn on the top of their head. They used RNA interference (RNAi) to perturb transcription of the insulin receptor (InR) – that is, they simply stopped this particular signalling pathway from working properly. They did this at the beginning of metamorphosis, a point when body size is no longer growing, but adult structures – such as genitalia, wings, and the huge sexually-selected horn – are. If increased cellular sensitivity to insulin / IGF signalling is at least partly responsible for the evolution of this exaggerated horn in these beetles, then horns should be more sensitive than wings to the experimental manipulation of the pathway activity via RNAi. Furthermore, Emlen and his team predicted that – just as with fruit flies – genitalia should be relatively insensitive to this disruption of insulin / IGF signalling.

Results showed that the genitalia of males whose InR pathway activity was disrupted did not show a significant reduction in size when compared to control males (which did not undergo the RNA interference treatment). Meanwhile, the wings of RNAi treatment males showed a significant reduction in size that measured around 2% in comparison to control males. This is typical of the majority of ‘metric’ traits, such as eyes, legs, etc. Horns, however, predicted to be the most sensitive to nutritional state, suffered a significant reduction of around 16% in RNAi treated males relative to control animals. This eight-fold increase in sensitivity of horns in comparison to wings is highly consistent with Emlen’s model of the evolution of exaggerated trait size from heightened sensitivity to this particular pathway – giving us a real insight into the black box of condition-dependence, and how such incredible traits evolved.

Note: I highly recommend reading the paper itself, not only because it’s very well-written, but also because Emlen does a great job of summarising models of sexual selection and condition-dependent traits, and the impact of this latest research on those models. Plus there’s some nice beetle pictures in there, and you love nice beetle pictures. DON’T YOU?

Read the Science paper here:

Emlen, D.J., Warren, I. A., Johns, A., Dworkin, I. and Corley-Lavine, L. (2012) A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science (in press).

Other references:

Rowe, L., & Houle, D. (1996). The lek paradox and the capture of genetic variance by condition dependent traits. Proc. Royal Soc. B, 263 (1375), 1415-1421.

Shingleton, A.W., Das, J., Vinicius, L. and Stern, D.L. (2005) The temporal requirements for insulin signaling during development in Drosophila. PLoS Biol. 3, e289.

Further reading:

Cotton, S., Fowler, K., Pomiankowski, A. (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proc. Biol. Sci. 271, 771.

Emlen, D.J. (2008) The evolution of animal weapons. Annual Review of Ecology Evolution and Systematics 39: 387–413.

Houslay, T.M., Bussiere, L.F. (2012) Sexual Selection and Life History Allocation. In: eLS 2012, John Wiley & Sons, Ltd: Chichester.

Shingleton, A.W., Frankino, W.A., Flatt, T., Nijhout, T.H., Emlen, D.J. (2007) Size and shape: The developmental regulation of static allometry in insects. Bioessays 29, 536.

That’s right, I did just recommend a review paper that I wrote. You should know by now that I’m absolutely shameless.