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Death by evolution: how a hapless adaptation aided in the untimely demise of a Lake Victorian fish

McGee M.D., Borstein S.R., Neches R.Y., Buescher H.H., Seehausen O., and Wainright P.C. A pharyngeal jaw evolutionary innovation facilitated extinction in Lake Victoria cichlids. Science. 27 November 2015. DOI: 10.1126/science.aab0800

But, it was all going so well!

You’re lost in a strange land far far away from home, but you’re totally unfazed because you’ve got that trusty map app to save you. Feeling like some sort of superhero, you reach into your pocket to grab your smart phone, but just as you swipe the screen your heart sinks—you’re out of charge and out of luck. Here you are in Times Square (for heavens sake!) holding one of the twenty-first century’s most innovative devices, and, yet, you are hopelessly and utterly lost, and somehow the thought of asking someone of the hundreds of people rushing past for directions is completely lost upon you.

In much the same way as technological innovations disrupt the way we lead our lives, evolutionary innovations enable species to access untapped resources to escape competition. While these morphological adaptations confer advantages (otherwise they wouldn’t stick), evolutionary innovations may come at a cost, often invoking an irreversible transition from a generalist strategy to a more specialized one. This might not matter in a natural ecological context, but come a sudden and catastrophic change and the specialist might just find itself out of luck and extinct.

Scientifically, fitness tradeoffs are difficult to demonstrate because they entail reconstruction of a picture of the evolutionary history of a modern day animal using its morphology as a metaphorical negative. One way to go about demonstrating an evolutionary tradeoff is to identify a recently extinct species with a well-documented past and a salient evolutionary innovation, and compare and contrast it to living species with the same innovation inhabiting different ecosystems. Remarkably, a multinational team of scientists led by Matthew McGee of the University of California, Davis has filled this tall order, cleverly demonstrating an example of a fitness tradeoff resulting from an evolutionary innovation. The team reports its findings in a recent issue of Science.

The story starts in the 1950s when British colonialists introduced a fish called the Nile perch to Lake Victoria, the largest of the African Great Lakes, leading to the mass extinction of a native cichlid that once dominated its waters as the top fish-eating predator. The great scientific innovation begins with a canonical example of evolutionary innovation known as pharyngognathy, which is a modification to the “pharynx” (the back of the throat).This modification allows fish to deliver a nut cracker-like bite, useful for crushing difficult-to-eat critters such as hard-shelled crabs. It has been speculated that a potential cost of pharyngognathy comes from the accompanying narrowing of the throat, which may lead to a limitation in the size of prey that a fish can handle efficiently.  It so happens that cichlids are pharyngognathous fish, while the Nile perch is a non-pharyngognathous fish. Since the Victorian cichlid evolved in the absence of other fish-eating competition, McGee et al. reasoned that pharyngognathy might have played a previously overlooked role in the rapid extinction of the Lake Victorian cichlid as a result of unfair competition with the more efficient Nile Perch.

Several unique features make the case of the Lake Victorian cichlid a tantalizing subject for the study of evolutionary tradeoffs. First, the British fishing industry that wrought the demise of the Lake Victorian cichlid in the 1950s maintained records of Lake Victorian fauna, allowing scientists to reconstruct an ecological history of Lake Victoria pre- and post- perch. Second, living counterexamples to the incompatibility of pharygognathy and non-pharyngognathy are common in shallow water marine environments where both classes of fish have coexisted for millions of years. Moreover, cichlids of Lake Tanganyika, another African Great Lake, have likewise coexisted with a non-pharyngognathous species closely related to the Nile perch for millions of years. These living ecosystems provide scientists just the “model systems” they need to test hypotheses on pharyngognathy and its effects on predatory proficiency.

To explore the evolutionary cost of pharyngognathy, McGee et al. constructed an evolutionary history of marine pharyngognathy by connecting the lineages of pharyngognathous and non-pharyngognathous marine fish from ecosystems where they coexist, into an evolutionary family tree. They then mapped dietary information on the evolutionary tree and estimated the “rates of transition” or rate of dietary change of different fish from a processing-intensive dietary strategy (i.e., hard to eat things) to a fish-heavy diet. Supporting the idea that pharyngognathy has evolutionary consequences on fish diet, McGee et al. found that fish that evolved pharyngognathy moved toward prey specialization at a far greater rate than their non-pharyngognathous counterparts. Once a fish goes pharyngognathous, it’s hard for it to go back.

To test the hypothesis that the physical constraint in the pharynx resulting from the transition to pharyngognathy might be the basis for the loss in fitness of pharyngognathous fish, McGee et al. correlated feeding data with the size of the “pharyngeal gape”, that space at the back of the fish’s throat that shrinks as a result of pharyngognathy. Compellingly, they found that pharyngeal gape correlated with prey handling time. That is, a pharyngognathous fish could sometimes take hours to consume a fish that took a non-pharyngognathous fish minutes to eat, demonstrating that pharyngeal gape is a critical determinant of the ability to successfully compete for food. McGee et al. further used statistical inference to demonstrate that a fish’s ability to consume fish is the most important determinant of its evolutionary fitness as compared to other ecological variables, supporting the idea that the Victorian cichlid was outcompeted for a common resource (fish) by the Nile Perch. Lastly, they note that jaw size has a strong correlation with a fish diet. Examining the Lake Victorian fauna pre- and post- extinction, they observe that the surviving fauna, including surviving cichlid species, have come to closely resemble the fauna of pharyngonathous fish living in Lake Tanganyika where cichlids and relatives of the non-pharyngognathous relatives of the Nile Perch have coexisted for millions of years. Hence, McGee et al. come full circle in demonstrating that the Nile perch outcompeted the dominant fish-eating cichlids in Lake Victoria, sparing only the less specialized species.

While the findings of McGee et al. do not contradict the utility of pharyngognathy, or for that matter the “wisdom” of evolution, they convincingly demonstrate a tradeoff between specialist strategy and species resilience. Moreover, their study highlights the importance of considering ecological context when contemplating ecosystem resilience to change, as well as bringing to the forefront the ability of human activities to wreak havoc by carelessly altering Nature’s course.




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