Urbanisation is changing the way birds sing

In 1800 only 3% of the world’s population lived in urban areas, yet as the industrial revolution picked up pace in the early 18^th and 19^th centuries the number of people moving from the countryside to work in the newly industrialised cities soared. By 1950 29% of the world’s population were living in cities and by 1985 this had grown to 42% while in 2025 it is estimated to that it will be over 60%¹. That is just 10 years from now. In highly developed nations such as those in Western Europe and North America the 50% threshold has already been surpassed which means that if you live in a western nation and do not live in a city you are in a minority.

Across the globe cities are expanding.

It’s not just where people choose to live that is rapidly changing either, but how many of us there are. The human population is currently expanding more rapidly than ever before and has grown from just a few hundred million people less than a thousand years ago to over 7 billion today, and this number is still rising². As the human population grows cities are expanding quickly to meet the need for additional housing while the surrounding countryside is farmed and developed ever more intensely to provide us with the food, water and other resources we need to live.

Human population growth from around 5 million people in 8000 BCE to over 7 billion today. (figure from Keinen and Clark 2012).

Naturally, many people are concerned about how we are going to continue to feed and clothe ourselves as populations continue to expand, but there is also a growing concern among many about how such huge numbers of people are affecting the environment and the animals that inhabit it.

For animals which depend on natural habitats such as forests, meadows, or wetlands to survive, the growth of urban areas often spells bad news as these habitats are removed and paved over to make way for new suburbs, factories and roads. In the UK numerous species have declined for just this reason. For example, the bittern, a close relative of herons, was once widespread in reedbeds and wetlands across the UK but is now confined to a tiny area of the south-east after its habitats were drained to make way for agriculture and urban developments.

While many species cannot survive in urbanised areas, others are able to tolerate moderate levels of urbanisation and may continue living within cities despite drastic changes to their habitats. Life in the city is not without its challenges however, even for the most adaptable and resilient of species. Cities typically contain different threats to rural areas such as an abundance of cats which are responsible for killing huge numbers of birds and small mammals⁴, and high levels of chemical⁵, light⁶ and noise pollution⁷ which all have negative impacts.

This all sounds bad, and it really is, but while many species suffer badly from the effects of increasing urbanisation and habitat loss, there are a few species that have been able to adjust remarkably well to life in urban areas. One group that has been particularly well-studied in this regard are the songbirds and over the past 15 years or so, biologists have discovered some fascinating behavioural adaptations which have allowed some species to become successful city dwellers.

Great tits are one species which are adapting to city life.

One of the most notable features of cities across the world is that they are incredibly noisy places. With heavy traffic, building sites, aircraft flying overhead and all manner of other sounds and distractions it’s a miracle anyone can hear anything at all. For songbirds however, all this noise is more than just a distraction, it can seriously affect their chances of finding mates and successfully reproducing and for males it is likely to affect how well they can defend their territories against rivals.

While we may find bird song pleasant to listen to (or annoying depending on how early in the morning it is), for songbirds it has a serious purpose. Males sing during the breeding season to attract females⁸ and to signal to other males that their territory is occupied and should not be entered⁹.

City noise can overlap and interfere with these signals making communication among birds difficult and unreliable. The background noise of a city is typically continuous low rumble concentrated at around 2kHz in frequency. Unfortunately for many birds this overlaps neatly with the frequency of their songs and this can make it difficult for other birds to hear them as they do not stand out from the irrelevant background noise.

Clearly this is a problem for birds which rely on song to communicate, yet research has revealed that birds have ways of overcoming this problem and one of them is to increase the frequency at which they sing so that their songs literally rise above the background noise and can be clearly heard.

Sonograms of rural (a) and urban (c) great tit song compared to the background noise of a city (b). You can clearly see that the urban song is a higher frequency than rural song and above the frequency of the city noise. (from Mockford and Marshall, 2009).

Evidence that birds sing at higher frequencies in noisy cities than they do in quieter rural sites has now been found in numerous species including great tits (Parus major)⁷, blackbirds (Turdus merula)¹⁰, European robins (Erithacus rubecula)¹¹ and song sparrows (Melospiza melodia)¹².

In great tits the difference in song frequency between urban and rural sites has been measured at 478Hz¹³ and tests have shown that this is enough to substantially improve the distance over which song can travel in urban environments before it degrades and becomes inaudible¹⁴.

Birds may also face challenging noisy conditions in natural environments too such as where running water or wind creates high levels of low-frequency noise and these naturally noisy sites have allowed scientists to confirm that it really is the noise in cities and not some other factor which is causing city birds to sing at high frequencies. Biologists Henrik Brumm and Hans Slabbekoorn recorded the songs of white-throated dippers (Cinclus cinclus) living around noisy fast flowing streams in Scotland and found that they call at frequencies well above that of the background noise and higher than usual for this species suggesting that dippers in this area have adapted their calls to suit their noisy habitat¹⁵.

Dippers close to noisy streams sing at a higher frequency than the background noise so their songs can be heard (from Brumm and Slabbekoorn, 2005).

The effect of natural background noise on song frequency has also been shown in African little greenbuls (Andropadus virens) which sing at a higher frequency in areas where the rainforest is merging with open grasslands (known as ecotone forests) than they do deep within the rainforest itself¹⁶. Analysis of these two habitats revealed that the background noise in the rainforest is largely concentrated at higher frequencies while in ecotone forests there is more low-frequency noise. By singing at a lower frequency little greenbuls within the rainforest can ensure that their song does not overlap with the higher frequency background noise found in rainforests, while by singing at a lower frequency little greenbuls in ecotone forests avoid the lower frequency background noise in their habitat.

The evidence that birds change the frequency of their songs as an adaptation to noisy conditions may seem quite conclusive but not everyone agrees. An alternative explanation for the observed frequency shifts is that higher frequency song is actually just an unavoidable and possibly unimportant side-effect of singing more loudly, and it is higher volume, not frequency, which allows birds in noisy environments to overcome the background noise¹⁷.

In support of this argument Erwin Nemeth and Henrik Brumm of the Max Planck Institute for Ornithology in Germany found that the typical increases in song frequency found in great tits and blackbirds may be too low to substantially improve signal transmission whereas small increases in song amplitude were found to increase the distance over which a bird’s song could be detected much more effectively¹⁸.

But why should song frequency increase when birds sing more loudly? Nemeth and Brumm suggest two possibilities. Firstly, the increase in frequency observed in songs in noisy environments could be a side-effect of what is known as the Lombard effect (named after the French scientist Étienne Lombard) in which animals unconsciously increase the volume and frequency of their calls when the level of the background noise rises.

Nightingales in Berlin sing loudly to ensure that they are heard.

The Lombard effect is known to occur in humans (this is why it might feel like you have to shout to be heard at loud parties) and has also been shown in both lab and field studies of songbirds. Lab experiments on elegant crested tinamous (Eudromia elegans)¹⁹, and budgerigars (Melopsittacus undulates)²⁰, have shown that these species both sing more loudly and at a higher frequency when background noise increases and the same result has been shown in the field in a study of Nightingales (Luscinia megarhynchos) in Berlin²¹.

A second reason why song frequency may increase when birds sing more loudly is that both the volume and frequency of bird songs depend on the same song producing organ which could limit how well birds can independently control frequency and volume. In birds this organ is the syrinx which is the bird equivalent of the mammalian larynx or voice box and is located at the base of the windpipe connected to the lungs. Birds produce song by forcing air at high pressure from the lungs through the syrinx causing membranes to vibrate creating sound. This sound can then be modified using numerous tiny muscles which alter the shape and tension of the sound producing membranes.

However, past studies of the avian vocal system have shown that without these tiny muscles altering the structure of the sound, both the frequency and amplitude of bird song unavoidably increase together. In other words, when birds sing louder they cannot help but also sing at a higher frequency²².

Of course, this may be totally irrelevant if birds are able to use muscles to independently control the frequency and volume of their songs but there is evidence to suggest that the frequency and volume of bird songs really are closely intertwined. One of the clearest examples of this comes from a study by Nemeth and his colleagues at the Max Planck institute who recorded blackbirds singing in sound-proof chambers and showed that volume and frequency really were strongly correlated¹⁷. When blackbirds sing more loudly they also sing at a higher frequency and this may be totally involuntary. Similar results have been found in other species including zebra finches (Taeniopygia guttata)²³ and song doves (Streptopelia risoria)²⁴ suggesting that this pattern may be widespread in birds as a whole.

When blackbirds increase the volume of the song they also sing at a higher frequency. (image credit Juan Emilio).

It has become very clear over the past few years that urban noise is causing bird song to change however, opinion is still divided on whether it is the frequency or amplitude changes that are most important to improving song transmission in noisy environments. It is possible that both have important roles to play in helping birds to adapt to noisy urban areas and hopefully future research will provide an answer to this question.

The study of how urban noise affects bird song is a very active area of research and there are many unresolved questions which are likely to be answered in the next few years. Most importantly we need to find out what the long-term impacts of urban noise are on bird populations. Although many species of birds do seem to be able to adapt to noise we do not know how the dramatic changes we are causing to their environments will affect them in the long-term. Furthermore, many species are not able to adapt to urban areas for numerous possible reasons. They may not possess the behavioural flexibility to cope with new environments or not they might not be physiologically capable of changes their songs or behaviour. That is why studies those discussed here matter, we are changing the planet in ways which have never been seen before and we know that many species are suffering as a result. The first step to protecting animals from these changes is to understand how they are affected and that is just what these studies aim to do.

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References

1. Kegel, B (2014).Tiere in der Stadt: Eine Naturgeschichte. Köln: DuMont Buchverlag. (In German).

2. Keinan, A., & Clark, A. (2012). Recent Explosive Human Population Growth Has Resulted in an Excess of Rare Genetic Variants. Science, 336 (6082), 740-743 DOI: 10.1126/science.1217283

3. Barnosky AD, Matzke N, Tomiya S, Wogan GO, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, & Ferrer EA (2011). Has the Earth’s sixth mass extinction already arrived?. Nature, 471 (7336), 51-7 PMID: 21368823

4. van Heezik, Y., Smyth, A., Adams, A., & Gordon, J. (2010). Do domestic cats impose an unsustainable harvest on urban bird populations?. Biological Conservation, 143 (1), 121-130 DOI: 10.1016/j.biocon.2009.09.013

5. Liker A, Papp Z, Bókony V, & Lendvai AZ (2008). Lean birds in the city: body size and condition of house sparrows along the urbanization gradient. The Journal of animal ecology, 77 (4), 789-95 PMID: 18479344

6. Miller, M. (2006). Apparent Effects of Light Pollution on Singing Behavior of American Robins. The Condor, 108 (1) DOI: 10.1650/0010-5422(2006)108[0130:AEOLPO]2.0.CO;2

7. Slabbekoorn, H., & Peet, M. (2003). Ecology: Birds sing at a higher pitch in urban noise. Nature, 424 (6946), 267-267 DOI: 10.1038/424267a

8. Baker, M., Bjerke, T., Lampe, H., & Espmark, Y. (1986). Sexual Response of Female Great Tits to Variation in Size of Males’ Song Repertoires. The American Naturalist, 128 (4) DOI: 10.1086/284582

9. Krebs, J., Ashcroft, R., & Webber, M. (1978). Song repertoires and territory defence in the great tit. Nature, 271 (5645), 539-542 DOI: 10.1038/271539a0

10. Nemeth, E., & Brumm, H. (2009). Blackbirds sing higher-pitched songs in cities: adaptation to habitat acoustics or side-effect of urbanization? Animal Behaviour, 78 (3), 637-641 DOI: 10.1016/j.anbehav.2009.06.016

11. McLaughlin, K., & Kunc, H. (2012). Experimentally increased noise levels change spatial and singing behaviour. Biology Letters DOI: 10.1098/rsbl.2012.0771

12. Wood, W., & Yezerinac, S. (2006). Song sparrow (Melospiza melodia) song varies with urban noise. The Auk, 123 (3) DOI: 10.1642/0004-8038(2006)123[650:SSMMSV]2.0.CO;2

13. Mockford, E., & Marshall, R. (2009). Effects of urban noise on song and response behaviour in great tits. Proceedings of the Royal Society B: Biological Sciences, 276 (1669), 2979-2985 DOI: 10.1098/rspb.2009.0586

14. Mockford, E., Marshall, R., & Dabelsteen, T. (2011). Degradation of Rural and Urban Great Tit Song: Testing Transmission Efficiency. PLoS ONE, 6 (12) DOI: 10.1371/journal.pone.0028242

15. Brumm, H., & Slabbekoorn, H. (2005). Acoustic communication in noise. Advances in the Study of Behavior, 35, 151-209 DOI: 10.1016/S0065-3454(05)35004-2

16. Slabbekoorn H, & Smith TB (2002). Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution; international journal of organic evolution, 56 (9), 1849-58 PMID: 12389730

17. Nemeth, E., Pieretti, N., Zollinger, S., Geberzahn, N., Partecke, J., Miranda, A., & Brumm, H. (2013). Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities. Proceedings of the Royal Society B: Biological Sciences, 280 (1754), 20122798-20122798 DOI: 10.1098/rspb.2012.2798

18. Nemeth, E., & Brumm, H. (2010). Birds and Anthropogenic Noise: Are Urban Songs Adaptive?. The American Naturalist, 176 (4), 465-475 DOI: 10.1086/656275

19. Schuster, S., Zollinger, S., Lesku, J., & Brumm, H. (2012). On the evolution of noise-dependent vocal plasticity in birds. Biology Letters, 8 (6), 913-916 DOI: 10.1098/rsbl.2012.0676

20. Osmanski, M., & Dooling, R. (2009). The effect of altered auditory feedback on control of vocal production in budgerigars (Melopsittacus undulatus). The Journal of the Acoustical Society of America, 126 (2) DOI: 10.1121/1.3158928

21. Brumm, H. (2004). The impact of environmental noise on song amplitude in a territorial bird. Journal of Animal Ecology, 73 (3), 434-440 DOI: 10.1111/j.0021-8790.2004.00814.x

22. Titze, I. R. (1994). Principles of voice production (pp. 279-306). Englewood Cliffs: Prentice Hall.

23. Cynx J, Lewis R, Tavel B, & Tse H (1998). Amplitude regulation of vocalizations in noise by a songbird, Taeniopygia guttata. Animal behaviour, 56 (1), 107-13 PMID: 9710467

24. Elemans, C., Zaccarelli, R., & Herzel, H. (2008). Biomechanics and control of vocalization in a non-songbird Journal of The Royal Society Interface, 5 (24), 691-703 DOI: 10.1098/rsif.2007.1237

Carnival of Evolution #75: A journey

It’s the start of a new month and that means it’s time again for the Carnival of Evolution and this time it’s a special one, the 75th edition! So all aboard as we journey once more through some of the best evolution based blog posts from around the web.

Our first stop is the History of Evolution so step out and enjoy the view, there are many good things to see here.

Did Darwin and Wallace plagiarise their ideas on Natural selection from an obscure book on Naval timber? George Beccaloni responds with a resounding “NO”!

Why were Darwin’s ideas accepted so quickly in Victorian England? Piers J. Hale thinks one reason is that they endorsed the liberal Whig politics espoused by great thinkers like ” Darwin’s Bulldog” T. H. Huxley.

Christian Wenande tells us about a treasure trove of Darwin’s barnacle specimens recently discovered in Natural History Museum of Denmark.

You may know that Darwin was good friends with Kew botanist Joseph Hooker but did you know that Hooker was the first person Darwin told about his evolutionary ideas which he described in a letter as ” like confessing a murder”.

What would the world be like if Darwin had never existed? Michal Meyer reviews a new book, Darwin Deleted, that asks just that question.

A treasure trove of Darwin’s barnacle specimens have recently been discovered in Denmark (photo credit: Natural History Museum of Denmark)

All aboard! It’s time to move on to our next stop, Evolutionary Ecology.

Greg Laden talks about a new paper published in Science which shows that dinosaurs have been shrinking for at least 50 million years giving rise to those animals we call birds.

Jonathan Weiner discusses the lifes work of legendary ecologists Peter and Rosemary Grant whose 40 years of research on Galapagos finches showed evolution in action in wild animals.

Why are there so many more species in some regions than in others? GrrrlScientist tells us about a fascinating new study which shows that as available niches fill up the rate of speciation slows down, or even stops.

New reasearch shows that two species of Brazilian ants may have evolved without geographic isolation, although not everyone agrees.

Over at The Loom Carl Zimmer talks about an ancient lineage of air-breathing fish called Bichirs which learn to walk better on land if they are raised out of water, even changing the structure of their bones to improve their walking abilities. This may provide clues as to how fish evolved to walk on land.

Travis Park talks about the evolution of penguins and why it is important to calibrate molecular clocks against the fossil record.

Did these two species evolve in sympatry? Mycocepurus goeldii (left) and Mycocepurus castrator (right) are sister species which occupy the same geographic area (image credit: Christian Rabeling, University of Rochester).

And that’s it for evolutionary ecology this time, now our journey must continue as we head into the wonderful world of Evolutionary Theory.

Evolutionary fitness is often misunderstood the mean “healthiest, strongest, biggest, fiercest, and/or fastest”. Fortunately Stephanie Keep is here to tell us what fitness really means.

Charles Goodnight discusses some of his own work showing that within populations similar individuals tend to cluster together to form groups and this may lead to speciation.

Ben Haller talks about the interactions between empirical and theoretical researchers and asks Should theoretical ideas drive new empirical work to look for the patterns and outcomes predicted by theoretical models?  Or should pure “natural history” observations of the real world drive new theoretical work to explain the patterns and outcomes observed?

Our journey is almost at an end but not quite! Hold tight, we have three more posts to go.

Creationist Michael Behe claims the vertebrate glucocorticoid receptor could not have evolved by darwinian means. Thankfully Larry Moran is on hand to dismantle Behe’s arguments which are neither new nor interesting.

Elena Giorgi provides us with a very topical post about her work using ideas based on the evolution of HIV to develop a vaccine for Ebola.

Bradly Alicea shows us some really neat models of breeding networks that could help us better understand how behaviour and physiology lead to structured genetic variation in populations.

And finally, microbes can evolve the ability to form antibiotic resistant biofilms. Luckily for us people like Elyse Hope are working on ways to thwart them so that we still have effective antibiotics.

                                                                                                                  

And now we come to the end of the line. We hope you had a pleasant journey and will travel with us again soon. The next Carnival will be held in October at Eco-Evolutionary Dynamics, if you would like to submit anything you can submit it on the Facebook page. You can keep up with the Carnival of Evolution via Facebook and Twitter.

Cooperative sperm, killer sperm and the competition for reproductive success

In the closing paragraph of on the origin of species Darwin famously said that nature was a war in which individuals struggle against each other and the environment for survival. However, while survival may be important from an individuals point of view, from an evolutionary perspective mere survival is not enough. Reproduction is what matters and success or failure at producing offspring is what determines an individual’s evolutionary success. Of course, survival is important too, but only when it leads to reproduction.

In most species the reproductive success of females is limited by the rate at which they can produce offspring. When a female is pregnant or carrying eggs she has no choice but to wait until she has given birth or laid her eggs before she can reproduce again, and this can take a long time. Males have no such constraints to their reproductive success and can potentially mate with hundreds of females over their lifetime and raise an enormous number of offspring. The only thing stopping them is that there just aren’t enough females to go around. This shortage of females coupled with the need to reproduce leads to intense, and often aggressive, competition among males for limited mating opportunities.

Male red deer (Cervus elephus) compete for mating opportunities by fighting

Male red deer (Cervus elephus) fight for their chance to mate by using their huge antlers to batter their rivals into submission, while male northern elephant seals (Mirounga angustirostris) grow to enormous sizes allowing them to dominate harems of many females and guard them against the advances of smaller, weaker males. Not all species are so aggressive in their tactics. Males of many bird species such as peacocks (Pavo cristatus) and birds of paradise produce fantastic and colourful displays with which they attempt to attract females, as do a large number of insects and fish. In these species, rather than fighting with each other, males try to out-perform and out-class each other in the hope that females will choose them while their rivals are left unwanted on the sidelines. This may seem a more peaceful strategy but make no mistake, although these males don’t actively fight each other the competition between them is every bit as intense as among more aggressive species.

Male peacock (Pavo cristatus) aim to attract females by out-performing the displays of rival males.

So fighting or displaying are two ways in which males can improve their reproductive chances, but what happens in species in which each female mates with lots of different males in quick succession? How is a male to improve his odds of being the true genetic father of the offspring? Well, as is often the case evolution has found a way and that way is called sperm competition (yes, really).

In species in which females mate promiscuously males compete not just for mating opportunities but also for direct access to eggs. In these cases competition between males happens after mating has occurred as the sperm of multiple males compete with each other within the females reproductive tract as they race towards the eggs. In species in which sperm competition is known to exist an incredible variety of different sperm adaptations have been found, all of which serve to improve the sperms chances of reaching the eggs first.

For individuals of many species adaptation to sperm competition simply means producing more sperm so as to swamp the sperm of their rivals and increase the odds that some of their sperm will make it to the eggs before anyone elses. For other species adaptation to sperm competition is more complex. For example, the wood mouse, Apodemus sylvaticus, has evolved sperm that have a hook-like structure on the head which allows them to intertwine with one another to form long sperm ‘trains’ which are much faster at swimming than individual sperm.

The sperm of the wood mouse (Apodemus sylvaticus). (a) Image of the sperm head with the hook clearly visible. (b) 50 sperm hooked together. (c) A clip from video footage of the sperm train. (d) Another view of the sperm train with an arrow and asterisk marking the position of hooks. (e) One sperm latching onto another. (f) Another view of a sperm hook. Image from Moore et al. (2002).

In a similar and recently discovered case, a team led by Morgan Pearcy of the Université libre de Bruxelles looked for evidence of sperm competition in the desert ant, Cataglyphis savignyi. The queen ants of this species mate with up to 14 males in rapid succession and store their sperm jointly in a special storage organ called the spermatheca. Only those sperm which make it to this storage organ have any chance of fertilising an egg and so competition for access to the spermatheca is intense. In response to this pressure C. savignyi males have evolved highly cooperative sperm that team up into bundles of 50-100 cells which can swim much faster than they could alone and so are better able to outcompete their rivals.

Sperm from the desert ant Cataglyphis savignyi work together to increase their swimming speed. Image from Pearcy et al, (2014).

It is not just the way sperm behave that can change due to sperm competition, the shape and function of sperm can change too. For example, Philip Byrne and his colleagues from the University of Western Australia found that in a group of Australian frogs those species under the most intense sperm competition produced sperm with the longest tails, possibly to improve their swimming speed. Other species known to have oddly shaped sperm include the water beetle Dytiscus marginalis which has sperm that fuse at the head into pairs with two tails, and the tiny fruit fly Drosophila bifurca which at 6cm long produces the longest sperm on earth.

Some species have taken a more sinister approach to sperm competition and have evolved infertile “parasperm” which contain enzymes capable of breaking down the sperm of rivals. A similar and fantastically named kamikaze sperm hypothesis has even been proposed for humans in which some sperm are adapted to kill the sperm of rivals rather than fertilise eggs. The evidence for this hypothesis is equivocal at best but given the adaptations that have been discovered in other species it is not entirely unbelievable. In fact, given the adaptations that have been discovered so far, almost nothing is completely unbelievable.

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References

Sperm competition by producing large quantities of sperm
Moller, A. (1989). Ejaculate Quality, Testes Size and Sperm Production in Mammals Functional Ecology, 3 (1), 91-96 DOI: 10.2307/2389679

Sperm trains in the wood mouse
Moore H, Dvoráková K, Jenkins N, & Breed W (2002). Exceptional sperm cooperation in the wood mouse. Nature, 418 (6894), 174-7 PMID: 12110888

Cooperative sperm in the desert ant
Pearcy M, Delescaille N, Lybaert P, & Aron S (2014). Team swimming in ant spermatozoa. Biology letters, 10 (6) PMID: 24919705

Sperm competition in Australian frogs
Byrne PG, Simmons LW, & Roberts JD (2003). Sperm competition and the evolution of gamete morphology in frogs. Proceedings of the Royal Society B: Biological Sciences, 270 (1528), 2079-86 PMID: 14561298

The two tailed sperm of the water beetle
Mackie JB, & Walker MH (1974). A study of the conjugate sperm of the dytiscid water beetles Dytiscus marginalis and Colymbetes fuscus. Cell and tissue research, 148 (4), 505-19 PMID: 4836644

The world’s largest sperm in drosophila
Bjork A, Dallai R, & Pitnick S (2007). Adaptive modulation of sperm production rate in Drosophila bifurca, a species with giant sperm. Biology letters, 3 (5), 517-9 PMID: 17594959

Killer ‘parasperm’
Buckland-Nicks, J. (1998). Prosobranch parasperm: Sterile germ cells that promote paternity? Micron, 29 (4), 267-280 DOI: 10.1016/S0968-4328(97)00064-4

Kamikaze sperm
Baker, R., & Bellis, M. (1989). Elaboration of the Kamikaze Sperm Hypothesis: a reply to Harcourt Animal Behaviour, 37, 865-867 DOI: 10.1016/0003-3472(89)90074-2

Criticism of the kamikaze sperm hypothesis
Moore, H., Martin, M., & Birkhead, T. (1999). No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proceedings of the Royal Society B: Biological Sciences, 266 (1436), 2343-2350 DOI: 10.1098/rspb.1999.0929

A spider that masquerades as a bird dropping

The power that natural selection has to sculpt both the appearance and the behaviours of creatures so that they intricately and precisely fit their respective environments is for me a source of endless fascination and wonder. Some of the most impressive examples of natural selection’s power lie among the mimics of the insect and spider world where a huge diversity of body forms are to be found, from insects which look uncannily like leaves or moss, to spiders that look just like ants. The benefits of these disguises vary from species to species. For many blending seamlessly into the background provides some protection against predators, while for others it allows them to creep up on their prey unnoticed or lure victims to their demise.

The south-east Asian orb-web spider known as Cyclosa ginnaga is a perfect example of how mimicry may be used to conceal an animal from its predators, in this case highly aggressive predatory wasps. Although by themselves individuals of this species are conspicuously silver in colour and not all that well disguised, they are able to spin white circular silk decorations which they stand on in the centre of their webs as a way of concealing themselves. That might not sound like a great way to hide but the size, shape and colour of the spider when viewed against the white background of its decoration look remarkably like a bird dropping which, of course, is of no interest to predators. This type of mimicry, in which animals mimic inanimate objects, is termed masquerading and the details of this particular case were recently published in a new paper by Min-Hui Liu and colleagues.

a) Cyclosa ginnaga standing on its web decoration.
b) A bird dropping.
Photos from Lui et al. (2014)

Liu and colleagues wanted to know if the decoration of C. ginnaga really did function as an anti-predator masquerade. To test this the researchers first used a technique called spectral reflectance imaging to examine how the spider and its decoration appears through the eyes of its predators. After all, what looks like a bird dropping to us may look completely different to a wasp. This method compared the way that light reflects from the body of the spider and its decoration to what is known about the sensitivity of insect eyes. The results were unequivocal, wasps cannot see the difference between bird droppings and the masquerade display of C. ginnaga.

A composite picture showing examples of Cyclosa ginnaga on its web on the second and fourth rows and bird droppings on the first and third rows. Image credit: Min-Hui Lui.

The crucial test however, was to show that mimicking a bird dropping really does reduce the predation risk for the spiders and lead to real fitness benefits for individuals. To do this the researchers divided 39 wild caught spiders into three groups. To one group they coloured the bodies of the spiders black while leaving their decorations untouched, to another they coloured the decorations black while leaving the spiders themselves untouched, and to the final group they coloured both the bodies of the spider and their decorations black. They then observed the frequency of predator attacks on each group over 13 days and compared this to the predation rate on untouched spiders. From these three groups a huge increase in predation was observed on those spiders that had only their decorations blackened. This suggests strongly that having a white decoration really does help C. ginnaga to hide itself from predators.

Figure from Lui et al. (2014) showing rates of predator attacks when the spider, the spiders decoration, or both were coloured black.

As shown in the figure above, when both the spider and its decoration were blackened no increase in the frequency of predator attacks was observed. This is not so surprising as in this case the black spider is likely to be well camouflaged against its black background. What is surprising  however, is that when the spiders body was blackened but the decoration was not there was also no increase in predator attacks. This seems strange since a black body on a white background might be expected to stand out very clearly to predators. It may be that the wasps recognise only silver spiders as their target species and so don’t see the black coloured spiders as potential prey. It could also be that when a black spider is on a white background it still looks like a bird dropping since bird droppings often have black bits in them. The authors don’t discuss this anomaly in their paper but it does cast doubt on the idea that the silver spider in combination with the white decoration together form a masquerade which reduces the risk of predation. Nonetheless it is clear from this study that the web decoration does substantially reduce predator attacks, why that is so remains an interesting question that is open for discussion.

---

Reference

Liu MH, Blamires SJ, Liao CP, & Tso IM (2014). Evidence of bird dropping masquerading by a spider to avoid predators. Scientific reports, 4 PMID: 24875182

On June 10, 2014July 21, 2014 By Sam HardmanIn Behaviour, EvolutionLeave a comment

Coelacanths are not living fossils

The term ‘living fossil’ is often misleadingly used in the popular press to describe species which have, supposedly, stopped evolving. Commonly cited examples include horseshoe crabs, Ginkgo trees, hagfish and, perhaps the most famous of all, the coelacanths, a group of lobe finned fish with a very long evolutionary history of which two species still survive in the deep waters of the West Indian Ocean.

A modern-day coelacanth (Latimeria chalumnae)

Coelacanths have long been known from the fossil record with the oldest specimen dating back to the Devonian period, some 400 million years ago. They were however thought to have gone extinct, along with many other animals, in the end Cretaceous mass extinction event. That all changed one day in 1938 when a South African museum curator named Marjorie Courtenay-Latimer discovered a coelacanth amongst the catch of a local fisherman. The discovery was a sensation, a fish that had been thought to have been extinct had been rediscovered 65 million years later, it was not extinct! It was alive! It was amazing!

That’s how the story goes at least, and ever since it’s discovery journalists have talked about the fish that has been “left behind by evolution”. But is this really true? Can a species really exist for a span of time so great that it will have seen ice ages come and go, mountain ranges form and the great super-continent of Gondwana break apart, and through all this not change at all? Over recent years a mountain of evidence has been steadily growing showing that this is in fact not the case, coelacanths, like any other species, are constantly evolving to adapt to changing conditions.

A comparison of the living coelacanths (genus Latimeria) with some of its extinct relatives. The morphological differences are striking. Image from Casane and Laurenti.

It is sometimes claimed that there is a low rate of change in coelacanth DNA and that this leads slow evolution. However, this idea is now being challenged by systematic studies of the coelacanth genome which do not detect slow rates of genetic change. In one study forty-four genes were analysed and no dramatic decrease in the rate of change compared to other species was detected. Furthermore, there is no known reason why coelacanths should have slowly evolving genomes. Their environment in the deep ocean, while relatively stable, is not particularly unusual and is inhabited by other species which are not considered living fossils. Another factor that may lead to a slow rate of evolution is a slow generation time, however, the reproductive rates of coelacanths are not thought to be particularly long. Finally, coelacanth populations are small, and small population size is known to increase the rate of genetic change within a species. We might therefore expect these species to be evolving rapidly, not standing still.

Probably the most widely held belief about coelacanths is that, even if they are genetically different, they look exactly the same now as they did millions of years ago. This belief is mistaken. No fossils are known for either species of surviving coelacanth or even for members of its genus, Latimeria. This suggests that the scientists responsible for classifying the fossil and living species consider the morphological differences so great the they should be placed in widely separated groups. In fact, there are significant differences in the body shape and structure of modern and extinct coelacanth species. These include changes in the number of vertebral arches and substantial differences in skull morphology. The swim bladder of coelacanths has also changed from being filled with oil in the extinct genus Macropoma, to being ossified in modern species, suggesting that the two groups lived in very different environments. Lastly, there are substantial differences in size, with modern coelacanths being three and a half times larger than their closest extinct relative (one and a half vs half a metre).

Comparison of the skeleton of modern and extinct coelacanths. A) Latimeria chalumnae (a modern species), B) Macropoma lewesiensis (extinct), C) L. chalumnae skull D) M. lewesiensis skull, E) Pectoral fins of L. chalumnae (above) and Shoshonia actopteryx (another extinct relative) (below). Image from Casane and Laurenti.

The view that coelacanths are ancient prehistoric fish which have stopped evolving has been around for a very long time. However, the evidence is now in and it shows that it is time to put this mistaken idea to bed.

                                                                         

For a comprehensive review of the evidence showing that coelacanths are not living fossils see: –

Casane D, & Laurenti P (2013). Why coelacanths are not ‘living fossils’: a review of molecular and morphological data. BioEssays : news and reviews in molecular, cellular and developmental biology, 35 (4), 332-8 PMID: 23382020

For the study analysing forty-four coelacanth genes see: –

Takezaki N, Figueroa F, Zaleska-Rutczynska Z, Takahata N, & Klein J (2004). The phylogenetic relationship of tetrapod, coelacanth, and lungfish revealed by the sequences of forty-four nuclear genes. Molecular biology and evolution, 21 (8), 1512-24 PMID: 15128875

For a contrasting study claiming slow molecular evolution in these species see: –

Amemiya CT, Powers TP, Prohaska SJ, Grimwood J, Schmutz J, Dickson M, Miyake T, Schoenborn MA, Myers RM, Ruddle FH, & Stadler PF (2010). Complete HOX cluster characterization of the coelacanth provides further evidence for slow evolution of its genome. Proceedings of the National Academy of Sciences of the United States of America, 107 (8), 3622-7 PMID: 20139301

The winner of the evolution video contest 2013

You may remember way back in April I wrote about some fascinating research showing kin-selection operating in the wild in slave ants, Temnothorax longispinosus. These ants were able to indirectly increase their fitness by attacking or neglecting the larvae of the slave-maker ants in whose nests they had been forcibly put to work. The authors of this study have since produced a cool video explaining their work and this has just won the National Evolutionary Synthesis Center (NESCent) Film Prize for 2013. It’s an excellent video and I’m sure you’ll agree well deserving of this award. The other entries for 2013 are not yet available online (I’m told they will be shortly) however you can browse the entries for 2011 and 2012 here. I haven’t watched them all yet but do post in the comments if there are any that stand out to you.

 

Five books for evolutionary biologists

Whenever I visit someone’s house, particularly the house of a fellow scientist, I like to browse their bookshelves, partly because I’m curious about what other people are reading and partly because I’m always on the lookout for new books to buy for my own collection. Another way I find out about new books is through other people’s blogs and websites, in fact some of my most visited blog posts have been book lists which I return to periodically when searching for new reading material. With that in mind I thought it was about time this blog had a book list, so here it is, the Ecologica top five books on evolution and behaviour. 1. On the Origin Of Species by Charles Darwin (Amazon). No list of books on biology would be complete without including Darwin’s seminal work outlining his theory of evolution by natural selection. Although great advances have been made in evolutionary theory since The Origin was first published in 1859, this book is still hugely important and influential and a must read for biologists of any stripe. If you want to fully understand evolutionary theory, or at least how the theory has developed since its formation, you must read this book.

2. The Selfish Gene by Richard Dawkins (Amazon). This book is a classic and a truly great work of science writing. Dawkins makes the case for selection acting on genes rather than individuals or groups. This idea may have been more controversial when this book was first published in 1976 than it is now, although with a recent resurgence in interest in group selection this book is still highly relevant.

3. The beak of the Finch by Jonathan Weiner (Amazon). This book documents the work of Peter and Rosemary Grant, two biologists whose research in the Galapagos islands has shown that, for the finches that live there, evolution is happening so rapidly that we can actually see changes occurring year by year. A fascinating book and one that I really enjoyed reading.

4. Wonderful Life by Stephen Jay Gould (Amazon). The late Stephen Jay Gould was a fantastic writer and populariser of science and this is one of his best known books. Gould discusses the pre-Cambrian fossils of the Burgess shale and their importance for our understanding of evolution. Some of his ideas have proven controversial but this is still a great book and well worth a read. For a response to Gould’s ideas you might also read The Crucible of creation by Simon Conway Morris (Amazon).

5. Why Evolution is True by Jerry Coyne (Amazon). Coyne presents a compelling argument that evolution is not just a theory but a fact. If you don’t accept that evolution is a reality then read this book and change your mind. You might also read The Greatest Show on Earth by Richard Dawkins (Amazon).

So that’s my list, what do you think? And what would you add to it?

Rebellion! Enslaved ants fight back against their captors

Parasitism is the most common lifestyle on earth, be it plant, animal or fungi virtually all species are affected by it. There is something that I find deeply fascinating about parasites. It’s their adaptations that I find so interesting. Perhaps more so than any other type of organism, parasites have been fine tuned by evolution to fit their particular niches with exquisite precision. Some, such as mosquitos and ticks, may simply extract nutrients from their victims leaving them largely unharmed. Others, such as the ‘zombie ant’ fungus Ophiocordyceps unilateralis are much more sinister and can manipulate their host’s behaviour for their own selfish ends. Brood parasites are altogether different but no less interesting. Rather than using their hosts as a convenient food source these freeloaders exploit the parental care of others so that they don’t have to pay the costs of caring for themselves. Cuckoos, which lay their eggs in the nests of other birds, are probably the best known brood parasites but they are by no means the only species to have happened upon this particular lifestyle.

This image shows the slave-maker, P. americanus, on the left and the host species T. longispinosus on the right.

Slave-making ants are brood parasites which have evolved the ingenious trick of capturing and enslaving the workers of other ant species, putting them to work in their own nests raising their pupae. In many cases the slave-maker workers themselves have become completely unable to perform essential tasks on the colony such as foraging, nest maintainance and caring for their young. They have instead become specialised at searching for and attacking the nests of host colonies in slave raids during which all adult ants are killed or expelled. The slave-makers then rob the larvae of their host, taking it back to their own colony where they will develop into slave workers in the slave-maker nest.

Attacks by slave-maker ants are frequent and destructive and so impose a high cost on their hosts. This has led to the evolution of defence mechanisms in the host species which help it to resist enslavement, these include enemy recognition, fighting abilities and rapid escape from the besieged nest. All of these defences are useful before enslavement however, it has long been thought that defense behaviours that benefit the ants after enslavement could not evolve since enslaved workers cannot escape and, more importantly, cannot reproduce. Without a means of passing on their genes to a new generation it was thought that any new trait that arose in enslaved ants that helped them to fight back would die with those ants and be quickly lost.

This is the way that evolution normally works, new traits that are beneficial increase the reproductive success of the individuals possessing that trait and so, over time, it spreads through the population. Without reproduction a trait cannot usually spread. There is however another way. Animals can increase their own fitness by behaving in a way that increases the reproductive success of other animals with which they share a large proportion of the same genes. This is called inclusive fitness or kin selection and is in fact what worker ants do all the time. Worker ants are sterile but they can increase their own fitness by assisting the queen who carries a lot of the same genes that they do*.

So what does all this have to do with slave-maker ants? Well it seems that enslaved worker ants aren’t so helpless after all. Tobias Pamminger and his colleagues studied the relationship between the slave-maker ant, Protomognathus americanus, and its host, Temnothorax longispinosus. They collected colonies of both T. longispinosus and P. americanus ants from the wild and raised them in the lab. They then compared the brood rearing success of free-living T. longispinosus to their enslaved counterparts. Their results, which have just been published in the journal Evolutionary Ecology, show that enslaved worker ants actively fight back against their captors by killing or neglecting their pupae,  a trait termed slave rebellion. As the authors say in their paper…

Instead of raising the brood of their social parasite P. americanus to adulthood, enslaved Temnothorax were observed to kill a large proportion of the slave-maker pupae either by direct attack or by neglect

Enslaved T. longispinosus attack the pupae of a slave-maker.

A startling difference was found in brood rearing success between the two groups. On average pupae in free-living T. longispinosus nests had a survival rate of 85% while for pupae in P. americanus nests, under the care of enslaved workers, this dropped sharply to only 45%.

Alternative explanations for this result were ruled out by the authors. One possibility was that conditions in the laboratory did not suit the slave-maker pupae resulting in high mortality. Another potential explanation is that the enslaved worker ants simply don’t provide the same level of care for the pupae of other species as they do for their own. Both of these explanations were rejected because the slave-maker larvae (the stage before pupae) developed normally with a high survival rate and were well cared for by the enslaved workers. In fact as the authors point out, larval stage ants require more care than pupae do and this was provided by the enslaved worker ants. It was only once the slave-maker larvae had reached the pupal stage that the slave rebellion trait was observed. In an earlier study the authors witnessed first hand healthy larvae being attacked and killed by enslaved workers. This is the smoking gun providing the final peice of evidence that the difference in pupal survival rates between the two species is not a result of the environment or general poor care but results from active attack behaviour by the enslaved worker ants.

A Temnothorax sp. colony. Credit: Alex Wild.

The results of this study clearly show that enslaved T. longispinosus workers attack and kill the pupae of the slave-makers, but how could a trait like this evolve when it is only used by sterile workers trapped in the nest of another species? Evidence suggests that kin selection is the answer. Genetic analyses revealed that in the wild, ants in nearby T. longispinosus colonies were closely genetically related to the ants enslaved in P. americanus nests. Tobias Pamminger and his colleagues suggest that by actively killing or neglecting slave-maker pupae the enslaved workers are able to reduce the size of nearby slave-maker colonies and so lower the risk of slave raids on colonies of their own species in the same area.

Here we have an example of kin selection in action. Although enslaved ants cannot reproduce and cannot directly benefit from killing the pupae of slave maker ants, they can benefit indirectly by reducing the impact of the slave-makers on nearby nests whose members carry the same genes that they do. This is they key point, natural selection acts on genes, not individuals. By behaving in a way they benefits copies of their genes in the bodies of free-living ants, enslaved ants were able to increase their own fitness and the slave rebellion trait was able to evolve.

*It’s actually a bit more complicated than this, ants have an unusual sex-determination system in which males carry only one copy of each chromosome while females carry two. This has all sorts of interesting implications which belong in a post of their own, see here if you’re interested.

                                                                                     

Pamminger T., Leingärtner A., Achenbach A., Kleeberg I., Pennings P.S. & Foitzik S. (2013). Geographic distribution of the anti-parasite trait “slave rebellion”, Evolutionary Ecology, 27 (1) 39-49. DOI: 10.1007/s10682-012-9584-0

The enigmatic fossa and the evolution of sociality

Madagascar is a land filled with wonderful creatures, from charismatic lemurs to chameleons so small they can stand on the tip of a pencil. It is also home to the fossa, Cryptoprocta ferox, a carnivorous cat-like mammal endemic to the island and thought to be closely related to mongooses (although this is contested). Unusually for a mammal, male fossas sometimes form long-term social groups of two, or occasionally three, individuals that work as a team when hunting allowing them to take down big prey such as some of the larger lemurs. Sociality clearly provides animals with major benefits, not only when hunting but also in terms of decreased predation risk and an improved ability to defend resources such as territory, food supplies or mates. However, there are also significant costs such as increased competition for food when supplies are low or for mates when mating opportunities are limited.  In most male mammals it seems that the costs of sociality outweigh the benefits. Although it is known from a few other species such as cheetahs and kinkajous, for male mammals to form long-lasting social bonds is extremely unusual, especially when the females are solitary, as is the case with the fossa.

As a general rule female social groups occur in response to the distribution of food in the environment, while male social groups form in response to the distribution of females. When food sources are clumped females tend to aggregate at feeding areas while males form groups around them. In contrast, when food is evenly distributed both sexes are expected to lead mostly solitary lifestyles coming together only to reproduce. The fossa then is a bit of an oddball. It is the largest carnivore in Madagascar preying on small to medium-sized animals, its food supply is evenly distributed and, as theory predicts, the females live solitary lives. Why then do some males go against theory and form social groups? It may be that more sociable males benefit not only from cooperative hunting but also from increased mating success.

The fossa’s mating system is unique among mammals. During the breeding season large numbers of males gather at traditional mating trees which are occupied by small groups of up to three females. This leads to fierce contest competition among the males for access to mates and reportedly intense sperm competition. Those males that are able to monopolise access to females and gain the longest copulations are likely to reap the benefits of increased reproductive success. It may be that those males that form social groups share access to females and so gain a reproductive advantage over their solitary counterparts. However, intense sperm competition and typically small litter sizes may also impose high fitness costs to individuals belonging to groups of unrelated males thereby constraining the evolution of sociality.

This image from Arkive shows the fossa mating tree.

The evolution of group-living from solitary ancestors has long been a hot topic in behavioural ecology. The unusual social behaviour of male fossas makes them an ideal study species for testing predictions about why sociality arose in the first place. Answering the question of why some male fossas go it alone while others form associations is the subject of recently published research by Mia-Lana Lührs and her colleagues.

Lührs and her fellow researchers were able to track and gather data on 22 wild male fossas between 2007 and 2010. They began by capturing individuals using live-traps and taking DNA, tissue and hair samples together with data on body mass and length, testis volume, and canine width. Some of these males were also fitted with GPS-accelerometer collars before release.

Since social groups of males were expected to move and hunt in synchrony, accelerometers were used to record when, and how vigorously, individuals were moving. This allowed the researchers to determine when their tracked males were moving and hunting and if they were hunting as a group or alone. In order to determine male mating success seven females were observed during the breeding seasons between 2007 and 2010 and the number and duration of copulations by known males recorded.

The results of this study are fascinating. Male fossas were found to exhibit two distinct phenotypes which differ according to social organisation. Those males that formed associations were found to be 38% heavier and 13% larger than solitary males, most likely due to differences in diet and an increased foraging efficiency. Dietary analyses revealed that the diet of social males contains larger and more agile bodied prey than solitary males and this has been linked to cooperative hunting. Data from associated males fitted with accelerometer tags shows that their movements, including movements typically associated with hunting, were highly synchronised, supporting the view that associated males hunt cooperatively. These results suggest that the benefits of hunting in a group may more than compensate for the costs of increased competition for scarce food resources. The physical superiority of social males may also grant them reproductive advantages as they are able to out-compete solitary males for access to females.

These boxplots shows the proportions of major mammal species in the diet of solitary (grey bars) and social (black bars) males. Prey species are sorted by size from left to right, largest to smallest. You can clearly see that the diets of the two phenotypes differ with social males consuming far more large bodied prey than solitary individuals.

Since males appear to benefit from sociality it is worth considering why females of this species do not also form associations. Lührs and her colleagues propose that the energetic costs of competition for food when communally raising offspring are too high, for female fossas it just does not pay to be social. This may also explain why males usually only associate in pairs and, when groups of three have been observed, one member is usually in very poor condition. There is a fine balance between the benefits of cooperation and the costs of increased competition, two’s company but three’s a crowd.

The increased competition that comes with sociality not only applies to food but also to mating opportunities. This raises the question of how associated males share these limited opportunities to reproduce. A likely answer is that the costs of competition are accounted for by inclusive fitness benefits. This does appear to be the case. In four out of six associations the males were found to be likely litter mates, presumably brothers. Furthermore, the only unrelated male associates in this study were found to share mating opportunities. This suggests that forming associations provides males with significant benefits whether they are related or not.

This raises one final question, if forming associated pairs is so beneficial to males then why are there still any solitary males at all? Why hasn’t natural selection removed solitary behaviour from the population? One possibility is that the solitary males that were observed did not have any litter mates and so are constrained in their opportunities to associate with a familiar male. Put simply, they are solitary because they had no choice. No male littermates were found for any of the solitary males observed in this study, supporting this conclusion. Another possibility is that solitary males represent an alternative life strategy maintained by frequency dependent selection. Lührs and her colleagues suggest that the small size of solitary males may allow them to extract small lemurs from tree-holes or rodents from burrows. This seems unlikely since, when it comes to competition for mates, solitary males are at a significant disadvantage. Interestingly, Lührs and her colleagues note that in some species inferior males invest relatively more in sperm competition by producing more sperm. In fossas however this is not the case and this suggests that, for fossas, going solo is not an alternative strategy. At present the view that solitary males occur due to a lack of littermates with which to associate seems the most likely.

                                                                                                                        

claimtoken-51352dc0d52f9Luhrs M.L., Dammhahn M. & Kappeler P. (2012). Strength in numbers: males in a carnivore grow bigger when they associate and hunt cooperatively, Behavioral Ecology, 24 (1) 21-28. DOI: 10.1093/beheco/ars150
(pdf)

A frog with teeth and the violation of Dollo’s law

In 1893 a Belgian palaeontologist by the name of Louis Dollo formulated his law of irreversibility which stated that evolution is not reversible. According to Dollo, structures that have been lost over evolutionary time (such as gills in mammals) cannot re-evolve. To put it in his own words: –

“an organism is unable to return, even partially, to a previous stage already realized in the ranks of its ancestors”

However, if there’s one thing you should know about biology it’s that rules almost always have exceptions and often it is these exceptions that are the most interesting areas of research. A paper published last year in the journal Evolution and written by John J. Wiens documents one such case, an apparent violation of Dollo’s law, the loss and re-evolution of teeth in the lower jaw of frogs.

The class amphibia is divided into three major groups; the little known caecilians, the salamanders and the frogs and toads. Of these groups both the caecilians and salamanders have teeth in their lower jaws, or mandibles. This is the ancestral condition that has been retained ever since the first amphibians pulled themselves from the water during the Devonian period. However, in the lineage leading to frogs and toads, the order Anura, mandibular teeth were lost at some point after it split from its sister group, the salamanders, between 225 and 338 million years ago. This is shown in the phylogenetic tree below.

Phylogenetic analysis of the amphibians showing the presence (red lines) and absence (blue lines) of mandibular teeth. This trait was lost in the Anuran clade at some point after its split from the salamanders 338mya. Taken from Wiens (2011). Click to enlarge.

This is where it gets interesting. If, as we know they were, mandibular teeth were lost in the frog lineage hundreds of millions of years ago then, according to Dollo’s law, they should be found in no species of frog alive today. But this is not the case. Gastrotheca guentheri, or Guenther’s marsupial frog, does possess teeth in its lower jaw, in fact it is the only living species to have this trait.

I couldn’t find an image of this species showing the mandibular teeth but this image shows what Gastrotheca guentheri looks like.

If you look closely at the phylogenetic tree at the top of this post you can see G. guentheri is buried deep within the Anuran clade indicated by an arrow (re-evolution of mandibular teeth). No other species within the genus Gastrotheca, or indeed any other species of frog, possesses these teeth which means that they must have evolved independently in G. guentheri relatively recently. What we have here is an anomaly, G. guentheri is a species that violates Dollo’s law.

Before we consider why teeth have re-evolved after such a long period of absence it is worth considering why they were lost in the first place. Although teeth play a crucial role in prey capture for most carnivorous animals, many frogs instead catch their prey with their tongues which they flip out and downwards over the lower jaw. Mandibular teeth are therefore not required for most frogs and may actually be a hinderance when it comes to catching their prey, this may explain why they were lost so long ago.

The tongue method of hunting is however, only effective for those species that feed on relatively small prey items such as insects. Some species of frogs tackle much larger prey (such as other frogs) and have evolved stiffer mandibles and large fang-like teeth in the upper jaw to facilitate this. A few of these species have even evolved tooth-like structures on the lower jaw known as odontoids or serrations, these are not actual teeth but serve a similar function. As Wiens points out, it is clear that for some species of frogs mandibular teeth would be a significant advntage when hunting. Why they have re-evolved only in G. guentheri and not in other species is not known but may be due to developmental constraints that limit the re-evolution of mandibular teeth in most species of frogs.

Wiens study used genetic data to estimate the divergence times of the major groups of frogs and to pinpoint the times at which mandibular teeth were lost and when they later re-evolved in the lineage leading to G. guentheri. His results show that teeth were lost between 338 and 225 million years ago didn’t reappear again until only 20 million years ago, thus they were absent for 200 million years at least and most probably much longer. Further research is required to reveal why it is that mandibular teeth have only re-evolved once and what constraints may be preventing their re-evolution in other species.

If there’s one thing we can take away from this study it is that Dollo’s law is not really a law at all but a rule. This means that while it is true in most situations there are exceptions as we have seen. Dollo’s rule then is really just a statement about the statistical improbability of complex traits evolving in exactly the same way in the same lineage twice. It’s still important but it is not a law.

                                                 

Wiens J.J. (2011). Re-evolution of lost mandibular teeth in frogs after more than 200 million years, and re-evaluating Dollo’s law, Evolution, 65 (5) 1283-1296. DOI: 10.1111/j.1558-5646.2011.01221.x