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 inFunctional 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.”
We managed to pull off a bit of a coup at Breaking Bio (again!), having snagged Professor Marlene Zuk to chat with us about her popular science writing, research on rapid evolution, and – of course – crickets! Thanks to Bug Girl’s slot over at Wired Blogs, you can also read more there, or simply watch the podcast below. Remember, if you don’t want to see our faces, subscribe to the podcast via iTunes!
And, if you want to see the kind of selection pressures that are causing the spread of the silent-wing mutation in these crickets, check out the video below (courtesy of Nathan Bailey):
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.
Before I depart these shores for a few weeks, allow me to take a quick opportunity to do some ranting. It’s against something that anyone working in the field of sexual selection will likely have done, and definitely will have seen. It’s predictable, it’s lazy; it’s also entirely innocuous and not something anyone should really care about. Therefore, I’m furious, I hate it, and it must be stopped.
I am talking, of course, about the use of pictures of peacocks on the opening slides of a presentation.
Oh, and sidling along apologetically shortly afterwards will likely be Darwin himself, and the famous quote from his letter to Asa Gray (preferably in a flowery typeface):
“The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!”
This is generally used to set the scene for discussion of Darwin’s idea of sexual selection, particularly in terms of female choice for spectacular males: that fantastic male ornaments exist because females prefer to mate with the best-ornamented males. However, you may have noticed that a reference never pops up onscreen whenever the speaker blithely proclaims that sexual selection explains the existence of the magnificent peacock’s feathers. Evidence for the influence of train-feather eyespots on male mating success is somewhat conflicted*, and, intriguingly, peacocks have actually been useful in providing evidence for the loss of male ornaments over time. Now, don’t go thinking that I’m about to get all Joan Roughgarden on the general principles of sexual selection, nor that I’ll join the creationist school of thought that a failure to find good evidence of something in a single species at a given time somehow disproves a large, well-studied theory with a mountain of evidence across a huge variety of taxa. It just seems to me that, given Darwin spent 20 years accumulating evidence with which to back up his theory of natural selection**, he was probably a bit of a stickler for data.
So, with what should we replace the magnificent peacock when discussing female preference for male ornaments? Well, first let’s set a little scenery of our own, by looking at the history of sexual selection theory. Darwin outlined his thoughts on the evolution of male traits for enhancing reproductive success in ‘On the Origin of Species’; he then detailed it thoroughly in 1871’s ‘Selection in Relation to Sex’, which was published alongside ‘The Descent of Man’ (criminally, some people still prefer to read the book on human evolution, which is INSANE). It attracted much interest, and no little criticism – particularly from Alfred Russel Wallace. While there are noble efforts going on just now to ensure that Wallace gets a little more of his deserved share of recognition for the theory of evolution by natural selection, he certainly had a far more dour view of the animal kingdom than did Darwin. In fact, Wallace’s views led to around a century in which sexual selection was sadly neglected – despite the occasional foray into theory by the likes of the great statistician Sir Ronald Fisher – and natural selection was treated as the only real mechanism behind evolutionary change.
Wallace’s raging adaptationism meant that he tried to ‘explain away’ colourful ornaments; the idea that a simple female preference could overcome the power of natural selection was anathema to him. For example, it was his belief that, in many birds and other species with ornamented males, the colourful state was ‘normal’, an unselected side effect from the greater ‘vigour’ of males in comparison to females (which he also used to explain male displays in the breeding season, during which they were – presumably – excessively ‘vigorous’!). The females, meanwhile, were selected to be camouflaged in order to protect the nest. Helena Cronin deals with this period in fantastic detail in her book ‘The Ant and the Peacock’, and provides a telling summary when she remarks that Wallace “excelled in understanding the dull, the drab and the dowdy”.
It was not until 1982 that female preference for ever more extravagant traits was explicitly tested, when the Swedish biologist Malte Andersson stepped out into the Kenyan grassland, armed only with a pair of scissors and a pot of glue. Many years before, Fisher had proposed that female preference might be such that it could push a male ornament into ‘runaway’ status, whereby it would continue to become exaggerated until finally curtailed by natural selection. Andersson had come up with an ingenious experiment that would finally test whether this hypothesis. He wandered out into widowbird territory, and caught himself a whole bunch of fancy males. Next, Andersson clipped the tail feathers from a group of these birds, and then glued a small length of feathers back onto them (making short-tailed males); he also glued remaining clippings onto the tails of others (creating super-long-tailed males). He also – in a classic lesson in experiment design – had two groups of ‘normal-length’ tails, in which one group had their tails cut off and then glued back on again. This was to check whether some part of that process could be responsible for results, not because Swedish biologists are unnecessarily cruel and unusual. The other control group was left alone, their tails unmolested. Then back into their marked territories they went, to display for watching females.
An hour after the birds were released, Andersson counted the number of nests on each territory; he then continued to inspect these territories for active nests on a weekly basis. An active nest is indicative of whether a female has mated with the male on that particular territory. Before having modified the tail treatments, Andersson had found only minor differences between the mating success of males, but afterwards he was struck by the huge increase in active nests of those males with elongated tails compared with all others. Having excluded territorial and behavioural differences (through randomisation, controls, and behavioural measurements), he concluded that females really were selecting males based on this seemingly arbitrary trait. Note that this experiment does not say why females were choosing the males with the longest tails, only that they were choosing them. The use of extra-long tails also showed that female preference went above and beyond the current range, as Fisher had hypothesised. The tail of the widowbird gave the first real evidence that male traits are favoured by female choice, and likely evolved through this mechanism.
But, back to my main point. Am I saying that we should simply replace all instances of peacocks with widowbirds? No, no I’m not. But when we talk about sexually selected traits, we’re often talking about weird ornaments, things that really shouldn’t exist, but do, and in “endless forms most beautiful and most wonderful”. We want to know why these things have evolved, in such varieties and with such incredible diversity. If we restrict ourselves to the same example over and over again, we are simply doing a disservice to the field in which we are privileged enough to work. Again, I point you to Malte Andersson, but this time to his wonderful 1994 ‘Sexual Selection‘ monograph; not only does he detail sexual selection theory from his well-placed vantage point, he also provides enough examples of well-studied, bizarre, intriguing animals to fuel your opening Powerpoint slide dreams for many conferences to come…
** remember, The Origin of Species was an ABSTRACT for the complete book that he had planned for his theory! If we have one thing to thank Alfred Russel Wallace for, it’s that he forced Darwin’s hand into this abridged version. I mean, come on.
UPDATE: below is my favourite response to this post so far…
That’s correct, friends – the two beetles you see in this image are both adult males of the same species of dung beetle, Onthophagus nigriventis. The chap on the right is clearly larger, and has a rather ostentatious horn extending from his thorax. This horn is a sexually-selected trait: horned males can use their armaments in battles over females, driving rivals away from mating sites, and even prying other males off a female whilst in flagrante. Sexual selection is all about the struggle to reproduce, and so traits are ‘sexually selected’ if their expression confers some benefit to the holder in terms of reproduction. In this case, large males with large horns are more likely to win battles with rivals, enabling them greater access to females, so there is a clear advantage to investing resources into weapons development.
Given that big, horned males fight rivals and guard their female partners (they may engage in the rather ungentlemanly pursuit of trapping lady beetles in mating burrows in order to have their way with them), then what the crap is going on with the guy on the left? Well, these horns are likely expensive in terms of resources, and any energy ploughed into growing horns is not available for investing in other traits – indeed, horns are known to trade off against morphological structures including eyes, antennae, and wings. Species of Onthophagus are well known for the size and diversity of their horns, but often these are only expressed by the largest ‘major’ males. What happens, then, if you’re a down-on-your-luck, resource-starved ‘minor’ male? Is there really any point in cashing in your precious metabolic chips for a gamble on a crappy little horn that’s never going to help you win any contests anyway? Surely there’s another strategy to be taken?
Indeed there is, and it’s called being a ‘sneaky fucker’*. While some males guard their mates, others will try to ‘sneak’ copulations with females. We now enter the realm of sperm competition: females may mate with multiple partners, so there is a battle amongst the sperm within her reproductive tract to fertilise eggs. If ejaculates are costly, males have to trade off resource investment on gaining fertilisation with investment on gaining additional matings. The more sperm ejaculated in a mating, the more eggs are likely to be fertilised – but, again, this requires resource investment. Furthermore, an increased risk of sperm competition should favour the evolution of increased expenditure on the ejaculate (i.e., the more likely that your little swimmers are going to be racing against some other dude’s, the more investment you should be making in ensuring your ejaculate is the biggest and best it can be).
In plain English (or, at least, an approximation thereof): if you’re a big horned dude protecting a little beetle harem, then you shouldn’t be all that worried about the fertilisation aspect – after all, you should be the only one for your ladies. You want to invest in lots of mating, not lots of ejaculate. Meanwhile, as a sneak, you’ve got to make those precious moments count, and ploughing your resources into the ejaculation makes sense – it’s in the female’s interests to have a few flings behind the dung-balls, so the greater the ejaculate, the better your chances of gaining fertilisations. Of course, the best way to produce larger amounts of ejaculate is to invest more resources into testis development.
All of which leads us nicely to what I think is one of the most ingenious (albeit slightly harrowing, once you really think about it) experiments I’ve read about while studying up for my PhD. Leigh Simmons and Doug Emlen (yes, this is another Doug Emlen-related post) cauterised those cells on beetle larvae which produce the thoracic horns in O. nigriventis, manipulating investment by ensuring that they could not grow these weapons. When compared to a control group comprising beetles allowed to develop normally, the cauterised individuals not only grew larger in size, but also developed disproportionately large testes. These results revealed the metabolic trade-off between horn development and both body size and testis size, in line with predictions from evolutionary models of ejaculate expenditure.
But what does this mean for the two beetles at the top of the page? Well, there’s a general tip here: if you’re going to sneak around, you’d better have gigantic balls.
*I’ve been told that Geoff Parker coined this phrase, but have been unable to find a reference for this, and during googling I accidentally clicked on ‘images’ and.. yeah. I need to keep safe-search on in future.
This post is a slightly modified version of an earlier entry on my ‘Nature!Sex!TopTips!‘ website.
Research blogging reference:
Simmons, L., & Emlen, D. (2006). From the Cover: Evolutionary trade-off between weapons and testes Proceedings of the National Academy of Sciences, 103 (44), 16346-16351 DOI: 10.1073/pnas.0603474103
Blatant plug: I am really interested in the intersection between sexual selection and life-history allocation – the way that individuals invest their resources – and (along with my long-suffering supervisor) have written an article on this topic for Wiley-Blackwell’s Encyclopedia of Life Sciences online journal. You can find it at the following link, or drop me a line if you would like a copy:
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.
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.
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?
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.
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?
For males, fitness depends on reproductive success: this requires that a male find a mate, ensure that his sperm fertilises her eggs, and that the subsequent offspring are viable. I have a tendency to focus on the first ‘episode’ of selection, given that I can then post photos of fancy traits, although this has led to my dabbling in sperm now and again (did I really just write that?). Thankfully, the Pitnick Lab at Syracuse University is all about sperm – to the extent that Scott Pitnick himself has a ridiculously awesome sperm-inspired tattoo, which you may have seen in Carl Zimmer’s ‘Science Ink’ book. His research includes investigation of sperm competition, where the sperm from multiple males competes within a female’s reproductive tract to fertilise her eggs.
Sperm competition has itself led to the evolution of different morphologies and tactics in both males and females (check out a preview of Leigh Simmons’ book here to find out more), but the particular research I want to look at here concentrates purely on tackling the problem of discriminating between the competing sperm of different males. Although it is now easy enough to mate a female with two males, and figure out the proportion of offspring sired by the second of these, we don’t really know what’s going on ‘under the bonnet’ (if that’s not too horrendous a euphemism). Research has shown that the last male to mate will usually sire around 80% of the offspring, but what are the mechanisms involved? Is it that the last ejaculate ‘displaces’ the previous? Do females ‘eject’ previous sperm?
The Pitnick Lab have found a way to investigate this, by using Drosophila melanogaster males which have been transformed so that they express a protamine in the sperm head that is labelled with either green or red fluorescent protein (GFP / RFP). These sperm can then be watched as they duke it out within the female’s reproductive tract, enabling researchers to figure out which of the hypothesised mechanisms are actually working in this system. Just in case, let’s recap. The video linked just below this paragraph (the website refuses to let me embed it, BOOOOoooo HISSSssss etc) is a female fruit fly’s reproductive tract. The red and green objects are sperm from male fruit flies who have mated with her. The reason that we can see that the sperm are different are because the fruit flies have been transformed so that their sperm are labelled with a particular protein. Oh, and green fluorescent protein was first isolated from a jellyfish, and is now routinely used to just, you know, show that some shit is happening. So bear with me while I repeat: SCIENCE IS AWESOME.