15 Gems of Evolution (Parts 12,13, and 14)

12) Darwin’s Galapagos finches

When Charles Darwin visited the Galapagos Islands, he recorded the presence of several species of finch that all looked very similar except for their beaks. Ground finches have deep and wide beaks; cactus finches have long, pointed beaks; and warbler finches have slender, pointed beaks, reflecting differences in their respective diets. Darwin speculated that all the finches had a common ancestor that had migrated to the islands. Close relatives of the Galapagos finches are known from the South American mainland, and the case of Darwin’s finches has since become the classic example of how natural selection has led to the evolution of a variety of forms adapted to different ecological niches from a common ancestral species — termed ‘adaptive radiation’. This idea has since been reinforced by data showing that even small differences in the depth, width or length of the beak can have major consequences for the overall fitness of birds.

To find out what genetic mechanisms underlie the changes in beak shape that mark each species, Harvard University’s Arhat Abzhanov and his colleagues examined numerous genes that are switched on in the developing beaks of finch chicks; their study was published in 2006. The researchers discovered that shape differences coincide with differing expression of the gene for calmodulin, a molecule involved in calcium signalling that is vital in many aspects of development and metabolism. Calmodulin is expressed more strongly in the long and pointed beaks of cactus finches than in the more robust beaks of other species. Artificially boosting the expression of calmodulin in the embryonic tissues that give rise to the beak causes an elongation of the upper beak, similar to that seen in cactus finches. The results show that at least some of the variation in beak shape in Darwin’s finches is likely to be related to variation in calmodulin activity, and implicates calmodulin in the development of craniofacial skeletal structures more generally.

The study shows how biologists are going beyond the mere documentation of evolutionary change to identify
the underlying molecular mechanisms.

Reference
Abzhanov, A. et al. Nature 442, 563–567 (2006).
Author websites
Clifford Tabin: http://www.hms.harvard.edu/dms/bbs/fac/tabin.html
Peter Grant: http://www.eeb.princeton.edu/FACULTY/Grant_P/grantPeter.html

13) Microevolution meets macroevolution

Darwin conceived of evolutionary change as happening in infinitesimally small steps. He called these ‘insensible gradations’, which, if extrapolated over long periods of time, would result in wholesale changes of form and function. There is a mountain of evidence for such small changes, called microevolution — the evolution of drug resistance, for instance, is just one of many documented examples. We can infer from the fossil record that larger species-to-species changes, or macroevolution, also occur, but they are naturally harder to observe in action. That said, the mechanisms of macroevolution can be seen in the here-and-now, in the architecture of genes. Sometimes genes involved in the day-to-day lives of organisms are connected to, or are even the same as, those that govern major features of animal shape and development. So everyday evolution can have large effects.

Sean Carroll from the Howard Hughes Medical Institute in Chevy Chase, Maryland, and his colleagues looked at a molecular mechanism that contributes to the gain of a single spot on the wings of male flies of the species Drosophila biarmipes; they reported their findings in 2005. The researchers showed that the evolution of this spot is connected with modifications of an ancestral regulatory element of a gene involved in pigmentation. This regulatory element has, over time, acquired binding sites for transcription factors that are ancient components of wing development. One of the transcription factors that binds specifically to the regulatory element of the yellow gene is encoded by engrailed, a gene fundamental to development as a whole.

This shows that a gene involved in one process can be co-opted for another, in principle driving
macroevolutionary change.

Reference
Gompel, N., Prud’homme, B., Wittkopp, P. J., Kassner, V. A. & Carroll, S. B. Nature 433, 481–487 (2005).
Additional resources
Hendry, A. P. Nature 451, 779–780 (2008).
Prud’homme, B. et al. Nature 440, 1050–1053 (2006).
Author website
Sean Carroll: http://www.hhmi.org/research/investigators/carroll_bio.html

14) Toxin resistance in snakes and clams

Biologists are increasingly coming to understand the molecular mechanisms that underlie adaptive evolutionary change. In some populations of the newt Taricha granulosa, for example, individuals accumulate the nerve poison tetrodotoxin in their skin, apparently as a defence against garter snakes (Thamnophis sirtalis). Garter snakes that prey on the newts that produce tetrodotoxin have evolved resistance to the toxin. Through painstaking work, Shana Geffeney at the Stanford School of Medicine in California and her colleagues uncovered the underlying mechanism; their study was published in 2005. Variation in the level of resistance of garter snakes to their newt prey can be traced to molecular changes that affect the binding of tetrodotoxin to a particular sodium channel.

Similar selection for toxin resistance apparently occurs in softshell clams (Mya arenaria) in areas of the North American Atlantic coast, as reported by Monica Bricelj at the Institute for Marine Biosciences in Nova Scotia, Canada, and her colleagues in the same issue of Nature. The algae that produce ‘red tides’ generate saxitoxin — the cause of paralytic shellfish poisoning in humans. Clams are exposed to the toxin when they ingest the algae. Clams from areas subject to recurrent red tides are relatively resistant to the toxin and accumulate it in their tissues. Clams from unaffected areas have not evolved such resistance.

Resistance to the toxin in the exposed populations is correlated with a single mutation in the gene that encodes a sodium channel, at a site already implicated in the binding of saxitoxin. It seems likely, therefore, that the saxitoxin acts as a potent selective agent in the clams and leads to genetic adaptation.

These two studies show how similar selective pressures can lead to similar adaptive responses even in very
different taxa.

References
Geffeney, S. L., Fujimoto, E., Brodie, E. D., Brodie, E. D. Jr, & Ruben, P. C. Nature 434, 759–763 ( 2005).
Bricelj, V. M. et al. Nature 434, 763–767 (2005).
Additional resources
Mitchell-Olds, T. & Schmitt, J. Nature 441, 947–952 (2006).
Bradshaw, H. D. & Schemske, D. W. Nature 426, 176–178 (2003).
Coltman, D. W., O’Donoghue, P, Jorgenson, J. T., Hogg, J. T. Strobeck, C. & Festa-Bianchet, M. Nature 426, 655–658 (2003).
Harper Jr, G. R. & Pfennig, D. W. Nature 451, 1103–1106 (2008).
Ellegren, H. & Sheldon, B. Nature 452, 169–175 (2008).
Author websites
Shana Geffeney: http://wormsense.stanford.edu/people.html
Monica Bricelj: http://marine.biology.dal.ca/Faculty_Members/Bricelj,_Monica.php

15 Gems of Evolution (Part 8)

8) A case of co-evolution

Species evolve together, and in competition. Predators evolve ever deadlier weapons and skills to catch prey, which, as a result of Darwin’s canonical ‘struggle for existence’, become better at escaping them, and so the arms race continues. In 1973, evolutionary biologist Leigh Van Valen likened this to the Red Queen’s comment to Alice in Lewis Carroll’s Through the Looking Glass, “it takes all the running you can do, to keep in the same place. If you want to get somewhere else, you must run at least twice as fast as that!” The ‘Red Queen’
hypothesis of co-evolution was born.

A problem with studying Red-Queen dynamics is that they can be seen only in the eternal present. Discovering their history is problematic, because evolution has generally obliterated all earlier stages.

Happily, Ellen Decaestecker from the Catholic University of Leuven in Belgium and her colleagues discovered a remarkable exception, in the co-evolutionary arms race between water fleas (Daphnia) and the microscopic parasites that infest them; their research was published in 2007. As the water fleas become better at evading parasitism, the parasites become better at infecting them. Both prey and predator in this system can persist in dormant stages for many years in the mud at the bottom of the lake they share. The sediments of the lake
can be dated to the year they were formed, and the buried predators and prey can be revived. Thus, their interactions can be tested, against one another, and against predators or prey from their relative pasts and futures.

Confirming theoretical expectations, the parasite adapted to its host over a period of only a few years. Its infectivity at any given time changed little, but its virulence and fitness rose steadily — matched at each stage by the ability of the water fleas to resist them.

This study provides an elegant example in which a high-resolution historical record of the co-evolutionary process has provided an affirmation of evolutionary theory, showing that the interaction of parasites and their hosts is not set in time but is instead the result of a dynamic arms race of adaptation and counter-adaptation, driven by natural selection, from generation to generation.

Reference
Decaestecker, E. et al. Nature 450, 870–873 (2007).
Additional resources
The Red Queen Hypothesis: http://en.wikipedia.org/wiki/Red_Queen
Van Valen, L. Evol. Theory 1, 1–30 (1973).
Author website
Ellen Decaestecker: http://bio.kuleuven.be/de/dea/people_detail.php?pass_id=u0003403

15 Gems of Evolution (Part 7)

7) Natural selection in lizards

A popular evolutionary hypothesis is that behavioural shifts in new environments negate the effects of natural selection. But work by Harvard University’s Jonathan Losos and his colleagues in 2003 lends little support to this theory. The researchers introduced the large ground-dwelling predatory lizard Leiocephalus carinatus to six small islands in the Bahamas, with six other islands serving as controls. They found that the lizard’s prey, a smaller lizard called Anolis sagrei, spent more time higher up in the vegetation on islands occupied by the larger predator than they did on the islands where L. carinatus was absent. But mortality in A. sagrei was still
much higher on the experimental islands than on control islands.

The presence of the larger predator selected for longer-legged male A. sagrei lizards, which can run faster, and also favoured larger females, which are both faster and harder to subdue and ingest. The researchers did not detect any selection on size in males; they suggested that the larger males may have been more vulnerable because of their conspicuous territorial behaviour.
The study shows how the introduction of a predator can cause individuals of a prey species to change their behaviour so as to reduce the risk of predation, but also cause an evolutionary response at the level of the population that differs between the sexes according to their ecology.

Reference
Losos, J. B., Schoener, T. W. & Spiller, D. A. Nature 432, 505–508 (2004).
Additional resources
Butler, M. A., Sawyer, S. A. & Losos, J. B. Nature 447, 202–205 (2007).
Kolbe, J. J. et al. Nature 431, 177–181 (2004).
Calsbeek, R. & Smith, T. B. Nature 426, 552–555 (2003).
Losos, J. B. et al. Nature 424, 542–545 (2003).
Author website
Jonathan Losos: http://www.oeb.harvard.edu/faculty/losos/jblosos

15 Gems Of Evolution (Part 2)

2) From water to land

The animals we are most familiar with are tetrapods — they are vertebrates (they have backbones) and they live on land. That includes humans, almost all domestic animals and most of the wild ones that any child would recognize: mammals, birds, amphibians and reptiles. The vast majority of vertebrates, however, are not tetrapods, but fish. There are more kinds of fish, in fact, than all the species of tetrapods combined. Indeed, through the lens of evolution, tetrapods
are just one branch of the fish family tree, the members of which just
happen to be adapted for life out of water.

The first transition from water to land took place more than 360 million years ago. It was one of the most demanding such moves ever made in the history of life. How did fins become legs? And how did the transitional creatures cope with the formidable demands of land life, from a desiccating environment to the
crushing burden of gravity?

It used to be thought that the first landlubbers were stranded fish that evolved to spend more and more time ashore, returning to water to reproduce. Over the past 20 years, palaeontologists have uncovered fossils that have turned this idea upside down. The earliest tetrapods, such as Acanthostega from eastern Greenland around 365 million years ago, had fully formed legs, with toes, but retained internal gills that would soon have dried out in any long stint in air. Fish evolved legs long before they came on land. The earliest tetrapods did most of their evolving in the more forgiving aquatic environment. Coming ashore seems to have been the very last stage.

Researchers suspect that the ancestors of tetrapods were creatures called elpistostegids. These very large, carnivorous, shallow-water fish would have looked and behaved much like alligators, or giant salamanders. They looked like tetrapods in many respects, except that they still had fins. Until recently, elpistostegids were known only from small fragments of fossils that were poorly preserved, so it has been hard to get a rounded picture of what they were like.

In the past couple of years, several discoveries from Ellesmere Island in the Nunavut region of northern Canada have changed all that. In 2006, Edward Daeschler and his colleagues described spectacularly wellpreserved fossils of an elpistostegid known as Tiktaalik that allow us to build up a good picture of an aquatic predator with distinct similarities to tetrapods — from its flexible neck, to its very limb-like fin structure.

The discovery and painstaking analysis of Tiktaalik illuminates the stage before tetrapods evolved, and shows how the fossil record throws up surprises, albeit ones that are entirely compatible with evolutionary thinking.

References
Daeschler, E. B., Shubin, N. H. & Jenkins, F A. Nature 440, 757–763 (2006).
Shubin, N. H., Daeschler, E. B., & Jenkins, F A. Nature 440, 764–771 (2006).
Additional resources
Ahlberg, P. E. & Clack, J. A. Nature 440, 747–749 (2006).
Clack, J. Gaining Ground (Indiana Univ. Press, 2002)
Shubin, N. Your Inner Fish (Allen Lane, 2008)
Gee, H. Deep Time (Fourth Estate, 2000)
Tiktaalik homepage: http://tiktaalik.uchicago.edu
Author websites
Edward Daeschler: http://www.ansp.org/research/biodiv/vert_paleo/staff.php
Neil Shubin: http://pondside.uchicago.edu/oba/faculty/shubin_n.html
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Gems from the fossil record
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NATURE|January 2009|doi:10.1038/nature07740
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