Released from predators, guppies reshape themselves—and their environment

A (domestic) male guppy. Photo by gartenfreuden.

ResearchBlogging.orgConsider a population of guppies living in the Aripo River in Trinidad. They have a happy existence, as far as guppies can be happy, but their lives are shaped by the constant threat of larger, predatory fish. The river runs clear over a colorful gravel bed, and guppies who stand out against that background are eaten quickly. Even guppies whose coloration helps them blend in have to be ready to make a break for it if a predator shows up. All in all, a guppy’s chances of surviving to mate depends most on its ability to hide from bigger fish, and to swim quickly when it can’t hide.

Then one fine day a biologist comes along, scoops up a couple hundred guppies, and moves them to a pool in a tributary of the river. The pool is separated from the mainstream by a series of waterfalls, so larger fish can’t swim up—the guppies are now free from their most dangerous predators. They can be fruitful and multiply. In this new habitat, camouflage and evasive maneuvers don’t matter so much. What does matter is finding enough food to make some babies in the midst of a whole bunch of other guppies who are also not particularly worried about predators.

John Endler started the experiment I’ve just described back in 1976 to see whether guppies’ coloration helps them hide from predators [PDF]. The guppies he moved to a predator-free stream have continued to evolve, though, and three decades later, new studies are showing how release from predators changed the guppies—and how those changed guppies could be changing the living community around them.

Since the 1976 introduction, Endler and other biologists have tracked the Aripo River guppies’ response to the change in natural selection he created. Release from predators is considered one of the classic sources of ecological opportunity that can free a population to evolve new traits and behaviors, and explore new ways of making a living. At the same time, a sudden lack of predators means that competition within the population can become stronger.

Points of measurement for guppy body and head shape, illustrated on a stained specimen. Image from Palkovacs et al, fig. 1.

In one study just published by PLoS ONE, Eric Palkovacs and two colleagues compared the body shape of guppies from the experimental population with guppies from the source stream. (Endler had noted changes in body shape along with changes in coloration in his original paper.) First, Palkovacs and his coauthors gauged how rapidly female guppies taken from each site snapped up standardized food. Then they killed the test fish, treated them with stain, and measured their body and head shape. Fish from the site with lower predation ate faster, and they had bigger mouths and deeper bodies than fish from the site with more predators.

Palkovacs and his coauthors also observed that the guppy populations at the experimental site were denser—without predators thinning them out, the fish are probably most limited by their food supply. A study published last year in PNAS suggests that this denser guppy population might reshape its own environment. The paper’s authors created artificial ponds stocked with algae and small invertebrates, then introduced guppies from the high-predation source site or from the low-predation experimental site. They also controlled for the differences in guppy population density associated with predator pressure, maintaining the fish at either the high density observed with low predation, or the lower density observed with high predation.

Where the guppies came from made a significant difference in the artificial ecosystems, and these differences were in some cases exaggerated by the increased population density caused by predator release. Guppies from the “released” site ate less selectively than guppies from the site experiencing higher predation, who favored invertebrates over algae. As a result, guppies from the released site were associated with less algae growth, and higher invertebrate population density. Probably because they ate more plant matter, guppies from the released site also excreted less nitrogen, reducing the nutrient’s availability for plant growth.

These results echo a study I discussed last year, which used a very similar approach to show that speciating sticklebacks can change their environment. It’s another reminder that evolutionary change can feed back to change the environmental conditions that prompted change in the first place—that natural selection operates in the midst of continuous change.

References

Bassar, R., Marshall, M., Lopez-Sepulcre, A., Zandona, E., Auer, S., Travis, J., Pringle, C., Flecker, A., Thomas, S., Fraser, D., & Reznick, D. (2010). Local adaptation in Trinidadian guppies alters ecosystem processes. Proc. Nat. Acad. Sciences USA, 107 (8), 3616-21 DOI: 10.1073/pnas.0908023107

Endler, J. (1980). Natural selection on color patterns in Poecilia reticulata. Evolution, 34 (1), 76-91 DOI: 10.2307/2408316

Palkovacs, E., Wasserman, B., & Kinnison, M. (2011). Eco-evolutionary trophic dynamics: Loss of top predators drives trophic evolution and ecology of prey. PLoS ONE, 6 (4) DOI: 10.1371/journal.pone.0018879

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When ecological opportunity knocks, does adaptive radiation answer?

ResearchBlogging.orgOne of the most basic questions in evolutionary ecology is, “why are there more kinds of this kind of critter than that kind of critter?” As in, why are there more than twenty thousand species of orchids, but only one species of ginkgo? Why are there hundreds of thousands of species of beetles, but only four species of horseshoe crab? In a literature review just released online—and my first publication as lead author!—my coauthors and I assess the support for one hypothesis: that species multiply because of ecological opportunity.

Biologists interested in the origins of species diversity frequently focus on the phenomenon of adaptive radiation, the process by which a single species rapidly gives rise to many new species, each with different traits adapted to different lifestyles. Darwin’s finches, with their beaks shaped to suit to different foods [$a], are a classic case; the Anolis lizards of the Caribbean, which have repeatedly evolved into a handful of “ecomorphs” with different body sizes and shapes adapted to different perching locations [PDF], are another.

Why are there so many [insert taxon here]? Photos by Bill & Mark Bell (1 & 2), fturmog (3 & 4).

The two most influential theories of adaptive radiation—by G.G. Simpson and Dolph Schluter—have suggested that it results when a species encounters ecological opportunity. Ecological opportunity might be a newly-evolved trait, or a new habitat, or the extinction of a species’ competitors or predators. For instance, a butterfly might evolve a way to overcome the chemical defenses of an abundant plant species, or a plant introduced by humans to a new habitat might find that local pathogens aren’t as deadly to it as the ones in its native range. Ecological opportunities have the effect of granting access to new resources. We have pretty good evidence that this can allow individual populations to increase in number, and even evolve greater diversity—but is that enough to spur the rapid speciation that forms adaptive radiation?

Ecological opportunity ? adaptive radiation

We’re pretty sure about steps 1 and 3. We’re still trying to figure out step 2.

Readers in certain demographic groups may think this sounds like an underpants gnome problem. But it isn’t, exactly. The gnomes’ business model can’t get to from step 1 (collect underpants) to step 3 (profit) because they don’t have a step 2. Evolutionary ecologists, on the other hand, already have their step 3 in the phenomenon of adaptive radiation. Ecological opportunity looks like a good prospect for step 1 precisely because it suggests some plausible options for step 2.

When a population encounters ecological opportunity, the new habitat, new trait, or extinction of antagonists provides access to new resources, and relaxes natural selection on the population. This leads to three phenomena usually grouped together under the term ecological release

  • The population experiences density compensation—more individuals can live in a particular area, creating stronger competition within the population.
  • Because of this stronger competition within the population, or because there isn’t much competition from other species, members of the population venture into new habitats, or use new food resources.
  • The population becomes more diverse, either because of the relaxed selection, or because of competition-driven selection for using new habitat and new resources.

One or more of these three aspects of ecological release turn up whenever populations find new food resources, or escape predators and/or competitors. Density compensation has been widely observed in populations colonizing new habitats, especially islands; and experiments with sticklebacks and fruit flies [$a] suggest that the stronger competition resulting from density compensation can spur the population to become more diverse in its use of resources. Bacterial populations can even evolve different specialized forms—adaptive radiations in microcosm—when introduced to new food resources.

Anoles show signs of density compensation on Caribbean islands—is that the reason behind their diversification? (Pictured: Anolis oculatus.) Photo via WikiMedia Commons

But where’s the speciation?

However, the evolution of bigger, more diverse populations is not the same thing as the evolution of new species—and that’s what adaptive radiation is really all about. These changes resulting from ecological opportunity might directly promote speciation if stronger competition leads to disruptive natural selection. Similarly, the competition-driven incentive to colonize new habitats or exploit new food sources could expose some parts of the population to different forms of natural selection, eventually causing them to evolve into specialists on the new resources. Finally, even if speciation only happens when natural barriers cut off migration, maybe larger, more variable populations provide more diversity for vicariance events to divvy up.

This is all pretty speculative, though. We still don’t know how often—or how rarely—divergent natural selection contributes to making new species. One way to deal with this is to approach the question from the other direction: look backward at the history of existing species, rather than following what happens to populations immediately after ecological release.

A backward-looking approach might use statistical analyses of the evolutionary relationships between living things to identify points in time when species formed unusually fast, and try to identify the cause. Some of my coauthors from the review paper recently published an analysis of the evolutionary tree connecting all vertebrates, and found that speciation rates increased around the origins of the largest group of birds, a large portion of the lizards and snakes, and non-marsupial mammals, among others.

This is very much a starting point, but maybe by complementing similar studies with research on populations currently evolving in response to ecological opportunity, biologists can work our way closer to understanding the origins of the endless and beautiful forms of life on Earth.

References

Alfaro, M., Santini, F., Brock, C., Alamillo, H., Dornburg, A., Rabosky, D., Carnevale, G., & Harmon, L. (2009). Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Nat. Acad. Sci. USA, 106 (32), 13410-4 DOI: 10.1073/pnas.0811087106

Bolnick, D. (2001). Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature, 410 (6827), 463-6 DOI: 10.1038/35068555

Blumenthal, D., Mitchell, C., Pysek, P., & Jarosik, V. (2009). Synergy between pathogen release and resource availability in plant invasion. Proc. Nat. Acad. Sci. USA, 106 (19), 7899-904 DOI: 10.1073/pnas.0812607106

Grant, B., & Grant, P. (1989). Natural selection in a population of Darwin’s finches. The American Naturalist, 133 (3), 377-93 DOI: 10.1086/284924

Kassen, R. (2009). Toward a general theory of adaptive radiation: Insights from microbial experimental evolution. Annals New York Acad. Sci., 1168 (1), 3-22 DOI: 10.1111/j.1749-6632.2009.04574.x

Losos, J. (1990). Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: An evolutionary analysis. Ecological Monographs, 60 (3), 369-88 DOI: 10.2307/1943062

Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University Press. Google Books.

Simpson, G.G. 1949. Tempo and Mode in Evolution. Columbia University Press. Google Books

Svanbäck, R., & Bolnick, D. (2007). Intraspecific competition drives increased resource use diversity within a natural population. Proc. Royal Soc. B, 274 (1611), 839-44 DOI: 10.1098/rspb.2006.0198

Wheat, C., Vogel, H., Wittstock, U., Braby, M., Underwood, D., & Mitchell-Olds, T. (2007). The genetic basis of a plant insect coevolutionary key innovation. Proc. Nat. Acad. Sci. USA, 104 (51), 20427-31 DOI: 10.1073/pnas.0706229104

Yoder, J.B., Des Roches, S., Eastman, J.M., Gentry, L., Godsoe, W.K.W., Hagey, T., Jochimsen, D., Oswald, B.P., Robertson, J., Sarver, B.A.J., Schenk, J.J., Spear, S.F., & Harmon, L.J. (2010). Ecological opportunity and the origin of adaptive radiations. Journal of Evolutionary Biology DOI: 10.1111/j.1420-9101.2010.02029.x

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