Evolution, climate change and coral

Increased carbon dioxide in the atmosphere poses several problems for organisms living in the marine environment. Increases in temperature and ocean acidification are the two best known and most worrying. In order to predict how climate change and ocean acidification will affect marine species, we need to know how they respond to these conditions. The effect of climate change on corals has attracted a lot of attention because of their importance for biodiversity.

We can't just expose corals to predicted conditions because corals of the future won't be naive to these environments and are likely to have evolved. We know that evolution can be extremely rapid, often within decades. Ignoring the potential for evolution to influence the effects of climate change on marine organisms could lead to inaccurate projections of the effects of climate change on extinction risk. Yet many authors are ignoring the effects of evolution and acclimation in making their predictions. 

The three-spine stickleback, Gasterosteus aculeatus has been documented adapting to freshwater conditions from saltwater ancestors in just 13 generations (photo Wikipedia)

In their 2007 paper, Hoegh-Guldberg, et al. dismiss the importance of evolution because "reef-building corals have relatively long generation times and low genetic diversity, making for slow rates of adaptation". But, long generation times are not present in all coral species and the response of corals to climate change is going to depend partly on their algal symbionts, which have short generation times. 

Unfortunately, the rates of evolution in corals and their symbionts are extremely poorly known. In terrestrial systems though, genetic variation for traits related to thermal performance is common and evolutionary responses to changing climate are typical. For instance, changes in allele frequencies consistent with responses to global warming have been documented in a number of insects, such as fruit flies and mosquitoes (e.g. Bradshaw & Holzapfel 2001, Umina et al. 2005).

Acclimation, or phenotypic plasticity, will also affect the way that corals respond to climate change. Plastic responses to the environment can occur within generations and across them. For instance, Donelson et al. (2011) looked at the tropical damselfish, Acanthochromis polyacanthus, and found that their offspring could completely compensate for the negative effects of higher temperatures. But, this only occurred when both they and their parents where reared at the same temperature.

The tropical damselfish, Acanthochromis polycanthus (photo Wikipedia)

There are indications that some acclimation is occurring in corals too. Under stress, corals expel their algal symbionts, which gives them the appearance of having been bleached. Coral reefs that experience greater variability in sea surface temperature and those that have recently been subjected to bleaching are less susceptible to bleaching. This greater resilience suggests that some acclimation to climate change is possible within short time-frames. 

A bleached coral in the foreground with an unbleached coral of the same species behind (photo Wikipedia)

We need a better understanding of how evolution and acclimation may influence the response of corals to climate change so that our predictions are accurate. But, we already know which direction things are probably going to go. John Pandolfi's work has shown that under historical climate change, diversity on corals reefs has declined and populations have moved to higher latitudes (e.g. Pandolfi et al. 2011, Kiessling et al 2012). 

Climate change is currently more rapid than previous episodes and this will limit the amount of adaptation that can occur. Corals are also already under significant pressure from other anthropogenic sources of stress that have resulted in substantial declines and changes in population composition. These pressures, too, will decrease the ability of corals to cope with the effects of climate change. By removing these pressures, we will give corals the best chance possible to adapt to a warmer and more acidic ocean.

Hoegh-Guldberg, O., Mumby, P., Hooten, A., Steneck, R., Greenfield, P., Gomez, E., Harvell, C., Sale, P., Edwards, A., Caldeira, K., Knowlton, N., Eakin, C., Iglesias-Prieto, R., Muthiga, N., Bradbury, R., Dubi, A., & Hatziolos, M. (2007). Coral Reefs Under Rapid Climate Change and Ocean Acidification Science, 318 (5857), 1737-1742 DOI: 10.1126/science.1152509  

Bradshaw, W., & Holzapfel, C. (2001). Genetic shift in photoperiodic response correlated with global warming Proceedings of the National Academy of Sciences, 98 (25), 14509-14511 DOI: 10.1073/pnas.241391498

Umina, P., Weeks, A. R., Kearney, M. R., McKechnie, S. W., & Hoffmann, A. A. (2005). A Rapid Shift in a Classic Clinal Pattern in Drosophila Reflecting Climate Change Science, 308 (5722), 691-693 DOI: 10.1126/science.1109523

Donelson, J., Munday, P., McCormick, M., & Nilsson, G. (2011). Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish Global Change Biology, 17 (4), 1712-1719 DOI: 10.1111/j.1365-2486.2010.02339.x

Pandolfi, J., Connolly, S., Marshall, D., & Cohen, A. (2011). Projecting Coral Reef Futures Under Global Warming and Ocean Acidification Science, 333 (6041), 418-422 DOI: 10.1126/science.1204794 

Kiessling, W., Simpson, C., Beck, B., Mewis, H., & Pandolfi, J. (2012). Equatorial decline of reef corals during the last Pleistocene interglacial Proceedings of the National Academy of Sciences, 109 (52), 21378-21383 DOI: 10.1073/pnas.1214037110

The aquatic ape hypothesis is rubbish

I mentioned the aquatic ape hypothesis in a recent post on wrinkly fingers improving grip when handling submerged objects. As if on cue, I then received this email:

Dear colleague,

Humans are very different from other primates, and many evolutionary hypotheses have been proposed to explain this remarkable fact. Is there scientific consensus on which of those hypotheses are most substantiated? If not, do opinions differ among researchers with different backgrounds?

Please help to establish the state of the art by answering a survey on this topic. You receive this invitation because you have recently published in a scientific journal covering paleoanthropology, paleontology or (human) biology, which indicates that you have expertise in a relevant field. 

A link to the survey is provided in the end of this message. 

Your responses will be anonymous. If you wish to be informed about the outcome of the survey, you can add your e-mail address to the mailing list after having completed the main survey. The present mailing list will only be used to send the invitations. My apologies if you receive this message more than once. 

Thank you for participating! 

Yours sincerely,
[Name and contact details redacted]

The first couple of pages were reasonable enough, containing questions on a variety of theories for how human traits evolved. Which is as you would expect from a survey that is trying to "establish the state of the art" on human evolution. But, the survey then degenerated into asking questions solely about the aquatic ape hypothesis. A quick bit of googling later and I find that the sender is a proponent of the hypothesis.

I am baffled by the persistence of the aquatic ape hypothesis. It has received almost no attention in the scientific literature because on more then superficial examination it fails to provide a parsimonious explanation of human evolution. In fact, to accept the aquatic ape hypothesis you would not only have to find its scant evidence convincing, but assiduously ignore the contradictory evidence.

Take the claim that bipedalism evolved in our ancestors as an adaptation to an aquatic conditions, from a situation much like how gorillas and chimpanzees walk when wading. It's a fine and very plausible claim, but it doesn't fit with what we know from the fossil record. All of the putative human ancestors, such as Australopithecus and Orrorin, retain features that show they were still capable tree climbers when they first started walking upright. For the aquatic ape hypothesis to be true, they would have had to come to the ground first then moved to water before becoming bipedal. There is nothing to support this in the fossil record.

Another problem that the human fossil record poses for aquatic ape proponents is that several of the traits claimed to be adaptations to aquatic conditions appeared separately. For instance, it's claimed that only a seafood diet rich in omega-3 fatty acids could support the expansion of brain size in the human lineage. Brain expansion, however, came after bipedal locomotion, indicating that the association with water had to have lasted several million years for both of these claims to be true.

Hairlessness is one of the traits that is central to the aquatic ape hypothesis. Again it is a fine and plausible claim to make, but hairlessness is poorly associated with an aquatic lifestyle. There are some notably hairless aquatic mammals, such as whales, dolphins and walruses, but there are many more aquatic animals that retain hair. Moreover, there are some hairless mammals that are clearly not aquatic, such as naked mole rats, rhinoceros[1] and elephants. Hairlessness is clearly neither necessary for an aquatic life nor is it uniquely associated with aquatic mammals.

A feature that is far more commonly associated with aquatic mammals is that they are testicond, that is they have internal testicles (at least the males do!). In fact, I know of no aquatic mammal that is not testicond. There are some mammals that are not aquatic and are also testicond, like our friends the rhinoceros and elephant[2], but the far more common condition for terrestrial mammals is to have external testicles. So, the external testicles of human males suggests that humans are typical terrestrial mammals and not aquatic apes.

There are a whole host of other features that aquatic ape proponents cite as evidence consistent with aquatic ancestry and it would take an entire website to debunk them all (like this one). Individually, none of these traits are very compelling evidence for their hypothesis, and taken together they're a complete mish-mash. While some are highly derived features, like hairlessness, others have barely changed from the ancestral condition, like webbing between the fingers.

More parsimonious explanations for the evolution of human traits involve multiple causes, not a single cause as proposed by the aquatic ape hypothesis. The aquatic ape hypothesis is neither simple[3], nor does it fit well with the available evidence. Proponents of the aquatic ape hypothesis need to bend the evidence to fit their hypothesis and resort to special pleading to explain away the inconsistencies in their arguments. It's a textbook example of adaptationist just-so storytelling.


[1] An interesting aside is that the species of rhinoceros that is most closely associated with water is often called the hairy rhinoceros.

[2] Another interesting aside is that both the rhinoceros and elephant are thought to have aquatic ancestors. The support for this is much stronger for the elephants, which are part of a clade (the Tethytheria) who's other members are all aquatic (the extant Sirenia and the extinct Desmostylia). This may explain why they and rhinoceroses are testicond. It does not explain their hairlessness, as we know that as recently as 10,000 years ago there were a number of very hairy rhinos and elephants, indicating that the common ancestors of modern rhinos and elephants were also hairy.

[3] The transition from arboreal to terrestrial to aquatic back to terrestrial is not a simple evolutionary scenario. A simpler assumption would be that human ancestors were all terrestrial after descending from the trees.

Ed Yong is treading on my turf

Ed Yong is treading on my turf (or should that be seagrass meadow?). Worse though, is that he is doing it better than me...

I have been writing a post about the longevity of coral reefs under future climate conditions. Yesterday, Ed (I hope I can call him that) posted a piece on the future prospects of retaining coral reefs into the next century. You should go read it, but come back in a few days when I post my own piece that will look at the issues from an evolutionary perspective.

*** UPDATE *** I've published my piece.

Online nature sound archive

Cornell University has just released their full archive, the World's largest, of bird calls and other animal sounds. It comprises nearly 150,000 recordings dating back to 1929. The Cornell press release says that they are trying to make the sound recordings as accessible as possible, to the broadest audience possible. If you're interested go check it out.

A first look at the giant squid footage

A fleeting glimpse of the footage of a live giant squid in its typical deep sea habitat, captured by filmmakers in Japan. You might want to watch it with the sound off...

A wrinkly hypothesis

The aquatic ape hypothesis was first proposed 70 years ago by German pathologist Max Westenhöfer. The hypothesis has more recently championed by Elaine Morgan, most notably in her book The Aquatic Ape. But the hypothesis has not drawn a lot of attention in the literature and has been dismantled in various places (here's one that's pretty good). Essentially the hypothesis interprets certain features, such as human hairlessness, as adaptations to an aquatic environment.

In 2011 Changizi et al. published a paper arguing that water-wrinkled fingers are an adaptation to life in aquatic environments. A new paper, just published, purports to test this hypothesis. Kareklas et al. had test subjects soak their hands in 40°C water for 30 minutes. Then they got the subjects to move marbles from a source container that was either filled with water or dry. The performance of the wrinkly handed participants was compared to a control group that performed the same task without soaking their hands.

Their results showed that the wrinkly finger group completed the marble moving task 12% faster when the source container was filled with water. There was no difference between the two groups when it was dry. They argue that their study shows a clear advantage to having wrinkly fingers when manipulating submerged items. But, I find the experiment completely underwhelming as support for wrinkly fingers as adaptations.

Most obviously, participants had to soak their hands in 40°C water for 30 minutes in order to obtain the small advantage. If wrinkled fingers are important for manipulating submerged objects, it seems to take an inordinately long time for fingers to wrinkle. Moreover, prior research has shown that lower temperatures, which are more likely to be encountered by our ancestors, result in slower and less exaggerated finger wrinkling (reviewed in Wilder-Smith 2004).

Marbles are also particularly small and slippery when compared with almost all conceivable objects that a paleolithic primate would be interested in picking up. It would be far more compelling if they had shown that the performance advantage remained when other objects were manipulated underwater. Given the very small advantage for marbles, I strongly suspect that the advantage would disappear for a vast array of other items.

The proponents of the aquatic ape hypothesis will probably incorporate the new study into their lists of evidence for a close association with with water in our ancestors. But, like most of their evidence, it is little better than plausible speculation dressed up as a compelling theory that deserves attention. It's a great way to get your ideas attention in the popular press, it's a horrible way to do science. The inoculation for such adaptationist nonsense is, as always, Gould and Lewontin 1979. 

Kareklas, K., Nettle, D., & Smulders, T. (2013). Water-induced finger wrinkles improve handling of wet objects Biology Letters, 9 (2), 20120999-20120999 DOI: 10.1098/rsbl.2012.0999 

Changizi, M., Weber, R., Kotecha, R., & Palazzo, J. (2011). Are Wet-Induced Wrinkled Fingers Primate Rain Treads? Brain, Behavior and Evolution, 77 (4), 286-290 DOI: 10.1159/000328223 

Wilder-Smith, E. (2004). Water immersion wrinkling Clinical Autonomic Research, 14 (2), 125-131 DOI: 10.1007/s10286-004-0172-4

Waterfall climbing fish

Diadromous fish are those that live part of their lives at sea and part of their lives if freshwater. Some of these fish reproduce in the upper parts of rivers above barriers like waterfalls, which they must scale in order to make it to the breeding sites. A newly published paper looks at how the Nopili goby, Sicyopterus stimpsoni, manages to climb waterfalls. The researchers found that the way the goby feeds and the way it climbs are very similar.

The Nopili goby, Sicyopterus stimpsoni (photo Takashi Maie)

During feeding the Nopili goby extends its upper jaw out much further and its lower jaw much less than other gobies. In climbing the basic motion is the same except the upper jaw maintains closer contact with the rock. Climbing is also assisted by pelvic fins fused into a sucker, a feature of all gobies. Because no other goby feeds in the same way, it's unclear whether the feeding or climbing movements evolved first.

The climbing galaxias, Galaxias brevipinnis (photo Robert McCormack)

There are many other fish that have a diadromous life-history, eels and salmon being the classic examples. There are fewer fish that climb waterfalls. However, in southern Australia and New Zealand there is a fish close to my heart that has a very similar life-history to the Nopili goby, but it climbs waterfalls in a different way. The climbing galaxias, Galaxias brevipinnis, climbs using its broad pectoral and pelvic fins and wiggling upwards.

Cullen J. A., Maie T., Schoenfuss H. L., & Blob R. W. (2013). Evolutionary Novelty versus Exaptation: Oral Kinematics in Feeding versus Climbing in the Waterfall-Climbing Hawaiian Goby Sicyopterus stimpsoni PLOS One, 8 (1) DOI: 10.1371/journal.pone.0053274

Flames under the sea

A survey to help locate sites for new marine protected areas has turned up perhaps the largest colony of flame shells, Limaria hians, anywhere in the world. The bed located at the bottom of Loch Alsh in western Scotland, contains at least 100 million individuals and covers 75 hectares.

The flame shell, Limaria hians (photo Wikipedia)

The flame shell is a bivalve mollusk that feeds by extending many orange tentacles out of its shell snaring food from the water column much like corals do. They grow to a maximum of about 4cm long, but most are around 2.5cm. Preserving flame shell beds is a conservation priority because they form nest-like structures that stabilise coarse sandy substrate giving other plants and animals a place to grow.