Thanks to the fine work of Cambridge’s Prof. Rebecca Kilner and her colleagues, in addition to her giving me access to her lab next year to photograph her beetles, today I have a photograph appearing in The Economist! The Kilner group have a new paper in the journal eLife that demonstrates how different levels of parental care have strong effects on offspring once they themselves have reached adulthood. I made the photograph above available via Creative Commons Attribution Licence so that it could be used in eLife, but The Economist wanted to use a different one, which they paid a licensing fee for (see below):
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?