Dirty Browsers – Determining a menu for North America’s fossil camels

The skeleton of the small, early camelid Poebrotherium on display at the American Museum of Natural History. Image from Wikipedia.

This is the fifth of eight posts on evolutionary research to celebrate Darwin's bicentennial.

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Life can sometimes be a futile contest. Throughout the natural world, pairs of species are locked in an evolutionary arms race where both competitors must continuously evolve new adaptations just to avoid ceding ground. Any advantage is temporary as every adaptive move from a predator or parasite is quickly neutralised by a counter-move from its prey or host. Coerced onward by the indifferent force of natural selection, neither side can withdraw from the stalemate.

These patterns of evolution are known as Red Queen dynamics, after the character in Lewis Carroll's Through the Looking Glass who said to Alice, "It takes all the running you can do, to keep in the same place." These arms races are predicted by evolutionary theory, not least as an explanation for sex. By shuffling genes from a mother and father, sex acts as a crucible for genetic diversity, providing a species with the raw material for adapting to its parasites and keep up with the arms race.

We can see the results of Red Queen dynamics in the bodies, genes and behaviours of the species around us but actually watching them at work is another matter altogether. You'd need to study interacting species over several generations and most biologists have neither the patience nor lifespan to do so. But sometimes, players from generations past leave behind records of the moves they made. Ellen Decaestecker and colleagues from Leuven University found just such an archive in the mud of a Belgian lake.

The lake is home to a small crustacean called a water flea (Daphnia magra) and a parasitic bacteria Pasteuria ramosa that lives inside it. Both species can undergo dormant states, and Decaestecker found that the lake's sediment preserves members of this sleeping fauna from up to 39 years ago. Every layer of sediment acts as a time capsule, preserving members from previous generations

Decaestecker sampled cylinders of sediment form the lake and revived dormant Daphnia eggs and parasite spores from different levels, representing intervals of 2-4 years. With these, she managed to hatch living Daphnia and pit them against parasites from their past, present and future.

On average, she found that the bacteria infected the water fleas more successfully if they came from the same time period than if they hailed from the past. As time went on, the bacteria picked up new adaptations that made them more effective parasites.

But Decaestecker also found that bacteria from a flea's future were also less infectious than its contemporaries. It seems that the parasites' upper hand is short-lived for the fleas evolve their own counter-adaptations. As the bacteria continue to adapt to the changing defences of their hosts, they trade-off the ability to infect the current generation with their ability to infect the previous ones.

This particular race isn't quite as one-sided as it might appear for slowly. Over time, the bacteria didn't become any better at infecting the water fleas, but those that did caused more virulent disease. They produced more reproductive spores and millions of these take up the fleas' bodies and effectively castrate them. Over time, the reproductive success of the infected fleas fell.

Reference: Decaestecker, E., Gaba, S., Raeymaekers, J.A., Stoks, R., Van Kerckhoven, L., Ebert, D., De Meester, L. (2007). Host-parasite 'Red Queen' dynamics archived in pond sediment. Nature, 450(7171), 870-873. DOI: 10.1038/nature06291

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Even with the young politician Jefferson Davis behind their adoption by the military, camels were a hard sell to the U.S. government. Along with other military men, Davis was convinced that camels could replace horses as the standard beasts of burden used by cavalry on the ever-expanding western frontier, but most congressmen and senators balked at the idea. When Davis tried to formally get a military appropriation for fifty camels (along with Arab trainers and other supplies) in 1851, the senators present for his speech thought the idea of cannon-carrying camels to be too frivolous to merit serious consideration, and the following year a similar request was similarly shot down.

But Davis was not to be deterred. The defeats the camel appropriation requests had suffered raised the idea’s profile, and when Davis took office as the U.S. Secretary of War in 1853 he renewed his push to see American soldiers riding camels across the arid western scrub. Once again, Davis’ attempt for an 1853 appropriation failed, but with some support from two midwestern senators, Davis was finally able to secure the $30,000 needed for the experiment. The “Camel Corps” project was made into law in March of 1855.

With the bureaucratic matters in order, Davis sent military officers out to the desert bordering the eastern edge of the Mediterranean Sea to gather information and procure dromedary camels to bring back to the United States. By the summer of 1856, a small herd had been offloaded and was being observed in Texas – even the local people, at first skeptical that camels could carry much weight at all, were impressed with the abilities of these animals to bear large burdens. Further tests confirmed that camels were adept at going over and through terrain which was impassible to horses and mules, and it seemed that Davis’ had been right about the utility of the camels.

Despite the promise the early observations held, western military outposts were not as enthusiastic about receiving the camels. The quartermasters preferred horses, and the soldiers disliked the Arab camel caretakers even more than the camels themselves. Nevertheless, those soldiers who did use camels found them to perform as well – if not better – than horses when traveling through the desert, and the experiment continued even after Davis left office in 1857. Then came the Civil War. When the Confederacy, led by Davis, broke away from the federal government in 1861 the camel experiment was effectively halted. Many of the animals were sold off, some were set loose to go feral, and others remained at their military outposts, causing a fuss among local people who thought them to be ugly, smelly nuisances (at least until Confederate troops captured some of these outposts and let the camels run off into the desert).

On its surface, the importation of dromedary camels to the United States would seem to be a government-facilitated invasion of a foreign species. Camels are animals of northern Africa and Asia, not North America. Yet, through the perspective of geologic time, the introduction of camels to the United States is no stranger than the importation of horses to the continent by European explorers. Much like horses, camels evolved in North America before being entirely extirpated from it; the introduction of modern species to the American west was something of a homecoming for a lineage which had been absent from it for more than 10,000 years.

Although the exotic camels brought to the United States acclimated well to life in the west, not all fossil camels lived in dry, scrubby habitats. Over the course of 45 million years many different genera of camels occupied an array of habitats, from closed forests to open grasslands. One way to appreciate this diversity – both of camels and the ecosystems they inhabited – is to look at the distinctive patterns of scratches and pits left by plant food on their teeth. As communicated in a new Palaeogeography, Palaeoclimatology, Palaeoecology paper, this is precisely what scientists Gina Semprebon and Florent Rivals have done.

The word “camel” is typically attributed to two species of mammal – the dromedary and Bactrian camels – but the extant camelids encompass a wider variety of creatures, including the llamas, alpacas, vicuñas and guanacos of South America. Despite their present range, though, for the first 36 million years of their evolution camelids were restricted to North America, with their heyday occurring around 16 million years ago during the Miocene (a time when many different large mammals, including horses and predatory whales, were also undergoing evolutionary radiations). By six million years ago, the llama and camel lineages had split and camelids had spread to other continents, and the remaining North American lineages became extinct at the end of the Pleistocene along with the giant ground sloths, mammoths, saber-toothed cats, and other megafauna. Although there are no endemic camelids left in North America, camelids persisted on this continent longer than any other, and so the fossil record of North American camelids provides a rich source of information about their paleobiology.

In order to ascertain the dietary habits of the extinct North American camelids, Semprebon and Rivals looked at three different aspects of their molars: the height of their teeth (the higher the tooth crowns, the rougher the diet), mesowear (wear on tooth cusps caused by long-term feeding patterns by an individual), and microwear (pits and scratches made by food during the time shortly before the death of the animal). Together these three different kinds of data outline not only the dietary preferences of individual animals, but also shifts in dietary patterns over time, which are themselves signals of the kinds of environments inhabited by camelids at different points in earth history.

After surveying tooth characteristics in a range of camelid taxa – from the small, early genus Poebrotherium and the giraffe-like, Miocene form Aepycamelus to the recently-extinct Camelops – Semprebon and Rivals found that, in general, fossil camels had much tougher diets than their living counterparts. In terms of mesowear, specifically, fossil camelids showed higher degrees of long-term wear on their teeth from the Eocene through the early Miocene. At this point there was a brief reversal in these trends, but after the mid-Miocene fossil camelids again showed increasing amounts of wear on their molars until the mid-Pleistocene, when there was another drop. Changes in tooth crown height roughly tracked this pattern – tooth crowns became higher during times when there were elevated degrees of mesowear on camelid teeth – indicating that for much of their evolutionary history camelids consumed tough, abrasive foods with reversals occurring in the mid-Miocene and from the mid-Pleistocene to recent time. In terms of tooth crown height and mesowear, living camels and llamas are more like early camelids than most of their fossil relatives.

Tooth height (hypsodonty; left) and mesowear (right) patterns for North American camelids during their evolution. Both graphs show significant dips in the Miocene - probably related to the availability of soft browse - before rebounding and dipping again during the Pleistocene to recent time. This graph sharply contrasts with W.B. Scott's idea of camelid progress from browsers to grazers over time. From Semprebon and Rivals, 2010.

This is the seventh of eight posts on evolutionary research to celebrate Darwin's bicentennial. It combines many of my favourite topics - symbiosis, horizontal gene transfer, parasitic wasps and viruses.

Blogging on Peer-Reviewed ResearchParasitic wasps make a living by snatching the bodies of other insects and using them as living incubators for their grubs. Some species target caterpillars, and subdue them with a biological weapon. They inject the victim with "virus-like particles" called polydnaviruses (PDVs), which weaken its immune system and leave the wasp grub to develop unopposed. Without the infection, the wasp egg would be surrounded by blood cells and killed.

Cotesiawasp.jpgThe wasps' partners in body-snatching are very different to all other viruses. Once they have infected other cells, they never use the opportunity to make more copies of themselves. They actually can't. To complete their life cycles, viruses need to package their genetic material within a coat made of proteins. In most cases, the instructions for building these coats are encoded within the virus's genome, but polydnaviruses lack these key instructions entirely. Without them, the virus is stuck within whatever cell it infects.

It's such a weird set-up that some scientists have questioned whether the polydnaviruses actually count as viruses at all or whether they are "genetic secretions" from the wasps themselves. Where on earth are those missing coat genes?

Annie Bezier form Francois Rabelais University has found the answer and it's an astonishing one. The viruses' coat genes haven't disappeared - they've just been relocated to the genomes of their wasp hosts.

In this way, the wasps and the viruses have formed an unbreakable alliance, where neither can survive without the other's help. Without the virus, the next generation of wasps would be overwhelmed by the defences of their caterpillar larders. Without the wasp, the virus would never be able to reproduce. Some viruses may be able to live happily alongside their host with little ill effect; others may even be beneficial in some way. But this is the first example of a virus co-evolving with its host in a compulsory binding pact.

Secret origins

The polydnaviruses were first observed in 1967 within the ovaries of parasitic wasps. From this storage facility, these biological weapons can be easily injected into a host, for the wasp's sting is just a modified version of her egg-laying tube. Bezier knew that when the viruses are first produced in the wasp ovaries, they come complete with coats, so the genes for building these must lie nearby.

She searched for virus-related genes that were switched on in the ovaries of two parasitic wasps from the braconid group - Cotesia congregata and Chelonus inanitus. It wasn't long before she found some - 22 potential genes that strongly resembled genes from another group of viruses called nudiviruses. Sure enough, some of these 22 genes encode proteins that form viral coats, and others encoded proteins responsible for assembling the virus particles together. These initial results strongly implied that the polydnaviruses are descendants of the nudivirus family .

Nudiviruses infect insects, so Bezier needed to make sure that the genes she was picking up hadn't just come from an infection that her wasps had picked up in her laboratory. Fortunately for her theory, she managed to find some of the same genes in eight species of braconid wasp collected from all over the world. And when she sequenced large tracts of C.congregata's genome, she found that at least 10 nudivirus-related genes had been fully integrated into the insect's chromosomes. These were no temporary hitchhikers - they were clearly stable parts of the wasp's genome.

Bezier went on to show that these nudivirus-related genes, hidden among the wasp genomes, were switched on when the adult wasps were still tucked away in their pupae. That's exactly the time when the polydnaviruses are first assembled. The genes are even switched on the exact spot in the wasp ovaries where the virus particles are produced. And to top it all off, Bezier found that 20 of these ex-nudiviral genes encoded proteins that make up part of the polydnavirus coat. It was the final proof she needed. The wasp genomes clearly contain ex-viral genes, which complete the assembly process that polydnaviruses can't finish themselves.

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Evolution of a partnership

The two wasps that Bezier studied hail from distantly related arms of the braconid family tree, which suggests that all the wasps of this group have nudiviral machinery incorporated into their genomes. Bezier thinks that the bond between wasp and virus was forged at least 100 million years ago, before the braconid wasp lineage had started to expand.

The genetic evidence suggests all the virus genes in today's wasps are the descendants of a single ancestral nudivirus that integrated itself into the genomes of an ancestral wasp. Many of these transferred genes are still incredibly similar across different species, suggesting that some aspects of the wasp-virus union are so important that they are resistant to change. Others have diverged more thoroughly and Bezier thinks that these are probably responsible for more specific interactions between virus and host.

In contrast, the polydnaviruses actually share very little of their own DNA. As an example, the strains used by C.congregata and C.inanitus hardly have any genes in common, even though their respective wasps use very similar coat-producing genes. Bezier thinks that many of the genes within the polydnaviruses aren't viral at all - they actually came from the wasp.

When the ancestral nudivirus infected the ancestral wasp, the two partners did a massive genetic swap, with wasp genes replacing viral ones and viral genes infiltrating the wasp genome. The virus has become a vehicle that allows the wasp to switch on its own genes within the body of a caterpillar. It's possible that this partnership was one of the reasons why the braconid wasps became such successful parasites and why today, there are at least 17,500 species of them.

Reference: Science 10.1126/science.1166788

Images: Photo by Alex Wild

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Given the patterns in tooth height and mesowear seen in other herbivorous mammals, it might be expected that many fossil camelids primarily fed on tough grasses. This does not appear to be the case. According to Semprebon and Rivals, most fossil camelids were actually browsers, but they foods they selected were tougher on their teeth. A prime example is the early Miocene genus Stenomylus. This long-limbed, antelope-like camelid had high-crowned teeth and appears to have been adapted to open, grassy habitats, but the patterns of microwear on its teeth are comparable to those of living herbivores which primarily browse on leaves. The reason for this seeming contradiction – a browser with the body of a grazer – may be that Stenomylus was a “dirty browser”, or ate soft plants covered in a significant amount of grit. If this was the case, then the high-crowned teeth of camelids were not adaptations to tough grasses, but to softer foods coated in bits of hard extraneous matter which could quickly wear down teeth.

W.B. Scott's simplified diagram of camelid evolution through time. This diagram mirrors early 20th century conceptions of horse evolution in that camelids were belived to have evolved from small browsers into large grazers. From A History of Land Mammals in the Western Hemisphere (1913).

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Blogging on Peer-Reviewed ResearchA child in the womb is not just some hapless creature waiting to be born into a world of experience. It is preparing. Through its mother, it senses the conditions of the world outside and its body plans its growth accordingly.

A mother's diet prepares her baby for life ahead.There is strong evidence that people who are under-nourished as embryos grow up to have higher risks of heart disease and other chronic illnesses. For example, people born to women during the Dutch Famine of 1945 had higher risks of coronary heart disease as adults.

We might nod our heads at this as if it were expected news, but it's actually quite a strange result. After all, during the early stages of pregnancy, the embryo is actually relatively undemanding. Any embryos that get off to an early slow start can easily catch up during the foetal stage, and they can certainly do it after birth. But Jane Cleal and colleagues from the University of Southampton have found, from studying sheep, that catching up may actually be the problem.

She divided several pregnant ewes into two groups and fed one on half the calorie intake of the other during the first quarter of their pregnancy. As expected, they put on less weight. Pregnant human teenagers often go through the same thing because they tend to be more active than older expectant mothers.

Lambs born to undernourished mothers weighed about the same as those whose mothers had it easy, but they packed on weight more quickly. And when the lambs were deprived of food between their third and sixth months of life, those that experienced poor nutrition in the womb bounced back faster than those that had it easier.

These results supports a theory that developing foetuses prepare for the world outside by using the health of their mother as a sort of nutritional barometer. If mum isn't getting much nutrients, the foetus steels itself for a life of hardship.

Lambs undernourished in the womb suffer health problems if they are well-fed after birth.In the case of the lambs, those that were under-nourished in the womb went through an initial growth spurt to give them a reserve to draw upon in times of anticipated hardship. And sure enough, they proved to be more resilient when such hardship did occur.

This is all perfectly sensible from an evolutionary point of view - after all, if mum can only afford to eat for one-and-a-half, life on the other side of the uterus is hardly going to be rosier.

But problems crop up when the foetus's intel is wrong - when nutrition before and after birth don't match up. Right from birth, it is poorly adapted to the world around it. The malnourished foetus that is born into a world of plenty is like a karaoke singer thrust into the spotlight at the Royal Opera House - unprepared and likely to do badly.

Cleal found that lambs that had poor nutrition before birth and plenty of food after it, might grow faster but not always in the right way. By their third year of life, they showed signs of poor blood pressure control and cardiac hypertrophy, a thickening of the heart's walls linked to a higher risk of heart disease and hypertension. Even their kidneys showed signs of weakness.

The potential harm of mismatched pre- and post-birth nutrition is particularly relevant for countries going through large spurts of economic development, or people emigrating to more affluent parts of the world. These mismatches could be made even worse by feeding newborn babies on calorific, high-fat diets, or weaning them onto unhealthy foods.

Other studies support Cleal's concerns. For example, Indian children who are small at birth and heavy at 8 years of age have higher levels of cholesterol later on in life, and higher risks of heart disease and diabetes. And children who are small at birth and put on lots of weight during development have higher risks of chronic diseases that those who are born heavy but grow more steadily.

Pre-adapting to the outside world has served us well in our evolutionary history. But in today's rapidly changing world, it might be contributing to the rising levels of heart disease, diabetes and other metabolic diseases in the Western world. The important next step is to find out exactly how this process works.

Reference: Cleal, Poore, Boullin, Khan, Chau, Hambridge, Torrens, Newman, Poston, Noakes, Hanson & Green. 2007. Mismatches pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood. PNAS doi:0610373104.

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Stenomylus was not an isolated oddball. Some camelids – such as the giraffe-like Aepycamelus – browsed on “cleaner” plant foods high off the ground, and camelid Megatylopus was a grazer, but, when looked at from a wider perspective, Semprebon and Rivals found that camelids moved into open habitats relatively early in their evolution and have primarily been dirty browsers in terms of diet. As far as teeth are concerned, the grit-covered foods camelids consumed caused their teeth to converge in form with those of grazers. This similarity has misled some paleontologists in the past. In his massive 1913 treatise A History of the Land Mammals of the Western Hemisphere, paleontologist W.B Scott wrote “The mode of evolution displayed by the camels does not differ in any significant respect from that seen in the horses,” and included an illustration showing how camels, too, evolved in a straightforward fashion from small browsers to large grazers. Now – thanks to the new study by Semprebon and Rivals and previous work on horses by paleontologists such as Bruce MacFadden – we know that neither camelids nor horses evolved in such a linear fashion, and camelids in particular have undergone some dental reversals as the available plant foods have changed during the past 20 million years.

So, although Jefferson Davis did bring camelids back to North America, the imported dromedaries were not equivalent to most of the camelids which lived on the continent during prehistory. The relatively narrow swath of modern camelid diversity does not contain an exact proxy for the species which have been lost from North America, and the feral camels which were loosed into the west interacted with the local flora and fauna in ways different from their prehistoric cousins. Seen in the context of their fossil relatives, though, modern camelids seem even stranger than they already are – they are evolutionary mosaics which the body of a grazer meets the diet of a browser.

Gina M. Semprebon and Florent Rivals (2010). Trends in the paleodietary habits of fossil camels from the Tertiary and Quaternary of
North America Palaeogeography, Palaeoclimatology, Palaeoecology, 295, 131-145 DOI: 10.1016/j.palaeo.2010.05.033

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