Category Archives: Sexual selection

Horny decisions, sneaky f**kers, and the importance of balls

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

Other references and further reading:

Simmons LW, Emlen DJ and Tomkins JL (2007) Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles. Evolution 61(11): 2684– 2692.

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

Parker GA (1990) Sperm competition games – sneaks and extra-pair copulations. Proceedings of the Royal Society of London Series B – Biological Sciences 242(1304): 127–133.

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:

Houslay TM, Bussiere LF. 2012. Sexual Selection and Life History Allocation. In: eLS 2012, John Wiley & Sons, Ltd: Chichester.

The original image is the copyright of Alexander Wild, an entomologist, photographer, and all-round great guy. You can find the original, and more of Alex’s work, at the links below:

http://www.alexanderwild.com/

http://myrmecos.net/

http://blogs.scientificamerican.com/compound-eye/

https://twitter.com/#!/myrmecos

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#Evol2012: Evolution 2012 review, special Doug Emlen edition

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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.

Fancy sperm

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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.

CLICK HERE AND LOOK AT THIS RIDICULOUS SHIT.

Here’s a different video so that I can embed something. It’s not quite as good, it only shows a FREAKING SPERM VORTEX:

I’m going to add to this post later, but for now I need to go and sit down.

WHAT THE HECK

SCIENCE

If you actually want to learn more while I go and try to get my head around it all, you can read the Science paper here:

Mollie K. Manier, John M. Belote, Kirstin S. Berben, David Novikov, Will T. Stuart, and Scott Pitnick (2010) Resolving Mechanisms of Competitive Fertilization Success in Drosophila melanogaster. Science 328 (5976)

There are more videos on the Pitnick Lab’s youtube channel.

Guest spot

Let’s talk about (cricket) sex

Of genetic variation and peacock spiders: Maratus volans and the lek paradox

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Maratus volans, photographed by Jurgen Otto

This month saw the long-awaited publication in PLoS ONE of a paper describing the courtship of the peacock spider Maratus volans, a tiny arthropod whose displays have helped it achieve the heady heights of internet fame over the past couple of years (well, at least in those parts of the internet where people like to watch videos of little animals dancing around). Girard and her fellow researchers used high-speed video recordings and laser vibrometry to show that male spiders use vibratory signals in addition to ornamentation and motion displays in order to attract a mate.

I have written previously on how males and females invest different amounts of resources in their gametes (sperm and eggs), and how this imbalance creates the conditions for sexual selection – Darwin’s proposed mechanism for the evolution of different body shapes and sizes across the sexes. Sexual selection covers both female choice and male competition, scenarios that have led to the development of exaggerated male ornaments and weaponry respectively (consider, for example, the beautiful train of the peacock, or the fierce antlers of stags).

While weaponry is used to fight or simply intimidate opponents (as well as the rather ungentlemanly acts of prising rival males from females mid-copulation, and trapping females in mating burrows, as is the wont of some beetles), ornaments serve to impress and seduce the watching female. Highly-ornamented species are often those in which both sexes mate with multiple partners, with males offering nothing more than their sperm – not for them the worries of caring for offspring, or providing food and territory for their mate*. The displays that males engage in often serve to highlight their ornaments – male greater sage grouse Centrocercus urophasianus are a prime example:

This type of behaviour is especially evident in ‘lekking’ species, where males gather on a display ground (the lek) and parade their wares to potential partners. Only those males with the very best ornaments are deemed good enough by the choosy females, and each will likely mate with multiple partners – meaning that the genes of a select few sires are making it into the next generation. This leads us to the essence of the ‘lek paradox’: if females are selecting males on the basis of certain trait values, this should erode genetic variation in these traits, meaning that all traits should converge to similar values. If all traits were the same, females would be unable to choose between males, and – more importantly – there would be no point in trying to do so. I like to remember this paradox through the reappropriation of the lyrics to a popular song:

However, there is plenty of evidence to show that female choice on the basis of sexual traits persists. So, how can we explain the maintenance of genetic variation for sexual traits? One proposed mechanism is that ornaments develop a strong relationship with an individual’s ability to acquire resources from its environment and convert them internally to usable forms – a relationship known as ‘condition-dependence’. This ability includes factors such as fighting disease, catching prey, foraging, and metabolising nutrients. All the genes underlying these factors are associated with the sexual trait due to condition-dependence, and so the trait serves as an indicator of how the vast majority of an individual’s genome is performing in its current environment. Rather than eroding the variation in a few genes that encode a trait, selection is now based on the vast variation of virtually the entire genome. Not only that, but changes in the environment will alter which genotypes perform best, and mutations in any area of the genome will have some effect on mating success.

While the paradox is named after lekking species, which often provide the most extreme examples of ornamentation, the problem extends to all those species where males do not give their partners direct (or ‘material’) benefits. Research in this field helps us to figure out the wider effects of sexual selection – for example, can it help to prevent the build-up of deleterious mutations in a population? On a different level, it is interesting to ask why such behaviour exists – is sex really worth the male making himself quite so obvious to predators? How does a female ‘know’ which male is ‘good enough’? This paper gives us a nice description of the courtship behaviour that we see in this video, and provides a basis for further study of these charismatic little animals (and others in the genus Maratus) – this is especially intriguing as the ‘multi-modal’ nature of their courtship is ripe for further investigation. Each facet is a drain on resources, whether it be the development of the colourful abdominal flaps and ornamented third legs, or the waving and dancing itself – to say nothing of the vibrational drumming, wonderfully described as ‘rumble-rumps’ by the paper’s authors. Why have the males evolved these multiple signals? Do they represent different features of his quality, and can females discriminate between them? Is one signal more important than all the rest? I’m sure I’m not the only one who’s excited about what else this colourful spider can inform us about evolution.

Get the paper here.

See more videos from the Elias lab at Berkeley here.

Check out Jurgen Otto’s fantastic photographs here.

*Note: I could not find much detail in terms of the mating system in Salticidae, much less this particular species, so it may indeed be that males are providing females with direct benefits. In which case, ignore me.

Check Mate

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A female decorated cricket, with spermatophore attached, dismounts male

Think of a duck. Chances are, you’re picturing a mallard – and, if you weren’t, you probably are now. Imagine the male with his striking green-blue head, and the comparatively drab, mottled brown female. If you are a regular reader of science blogs, or simply a fan of waterbird genitalia, your mind may wander to his 20cm-long explosive corkscrew penis, or her cavernous vagina, riddled with dead ends and hairpin bends.

The father of modern taxonomy himself, Carl Linnaeus – admittedly, without having gained privy to these reproductive organs – first classified the male and female mallards mistakenly as separate species. We accept these differences readily nowadays, but how and why have they occurred? Even stranger, why should any species evolve such elaborate reproductive organs?

The answer stems from ‘gametes’, or reproductive cells. Males are defined by carrying sperm, millions of pared-down parcels transporting genetic cargo at high speed. Meanwhile, females harbour relatively few eggs, sluggish monoliths packed with nutrients and protection, waiting patiently for one battling sperm to fuse the genetic information and produce a new organism.

This imbalance in the resources ploughed into gametes results in conflicting desires in the sexes. A male could incur little cost by mating with as many females as possible, increasing the probability of his genes passing to the next generation. His female counterpart, having invested so much in her eggs, gains more from exercising restraint to ensure her offspring are of the highest possible genetic quality.

By what means, then, can a female determine her perfect match? Darwin outlined such characteristics in his 1871 book ‘Selection in Relation to Sex’:

“…the greater size, strength, and pugnacity of the male, his weapons of offence or means of defence against rivals, his gaudy colouring and various ornaments, his power of song, and other such characters.”

This system can be as straightforward as the bull elephant seal using his great strength to drive rivals from a harem of females. Other traits proved far more puzzling – Darwin’s frustration in the years prior to this publication is summarised in an 1860 letter containing the epithet:

“The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!”

One theory is that such traits indicate genetic quality by acting like handicaps. Bright colours, displays and songs attract predators, while a cumbersome tail hinders a quick getaway. A male may be indicating, “Hey, if I have such a big handicap and I’m still here, doesn’t that show you how great I am? You should probably have my babies.”

What happens, then, to those that cannot compete at the highest level – should they simply give up? No, instead they engage in some downright sneaky behaviour, such as yellow dung flies waiting at the edge of a dung heap, ready to pounce on unsuspecting females travelling to meet Mr. Right atop a delicious pile of excrement. On the Hawaiian island of Kauai, Professor Marlene Zuk discovered that the mate attraction ‘song’ of the field cricket – produced by males rubbing their wings together – had enabled an invading parasitic fly to target the species ruthlessly. Rather than face extinction, however, this cricket population rapidly evolved to favour a mutation that removed rough edges from the wings. These smooth, silent crickets possess no real powers of attraction, instead surrounding the remaining chirpers in the hope of engaging a prowling female. While she would prefer a personal serenade from her potential mate, waiting too long exposes her to greater danger – or the risk of being ‘left on the shelf’. There is such a thing as being too choosy, after all.

Another tactic is to offer a ‘nuptial gift’, which can be an edible treat that the male produces himself. This has led to the synthesis of offerings that lower the female’s desire to remate before his sperm have completed fertilisation. ‘Aggressive sperm’ may outcompete or kill off rival gametes, while a dragonfly penis can scoop out existing seminal fluid. The bumblebee, meanwhile, breaks off its penis in the queen to form a ‘vaginal plug’ – an extreme case of putting all your eggs in one basket, if that’s not too confusing an analogy given the topic at hand.

It would be foolish to presume, however, that females have been standing by idly in evolutionary terms. Insects such as water striders and seaweed flies are locked in a race whereby females evolve anti-grasping functions just as the males develop claspers. Indeed, the mallard’s complex vagina has evolved as a defence mechanism. As the female is victim to frequent attempts at forced copulation, this not only helps to prevent entry, but also diverts unwanted sperm away from those precious eggs.

This arms race has raged ever since sex first evolved. As long as males and females continue searching for the tiniest advantage over one another, the battle of the sexes shows no sign of slowing down.

Tom Houslay

Insects // Sex // Evolution