According to an innovative exercise in 'morphospace analysis', modern fish owe their stunning diversity in part to an ecological cleaning of the slate by the mass extinction at the end of the Cretaceous.
Fish come in a bewildering diversity of shapes: trumpetfish, sea horses, pufferfish, cowfish and anglerfish are just a few examples. Size, too, varies tremendously in living species. Some gobies reach less than a centimetre as adults, whereas the oarfish stretches well over 12 metres and the ocean sunfish can weigh more than a car. These groups, along with almost two-thirds of all other fish, belong to a particularly conspicuous section of the fish tree of life, the spiny-finned fishes (Acanthomorpha). With 18,000 species, spiny-fins comprise almost a third of all vertebrates.
Despite, or perhaps because of, this incredible richness, biologists understand surprisingly little about the tempo of spiny-fin diversification. As he reports in Proceedings of the Royal Society, Friedman1 has searched for the origins and underlying causes of shape diversity in spiny-fins across nearly 100 million years of their evolutionary history.
A central challenge in macroevolution lies in explaining why biodiversity is unevenly distributed on the tree of life. Evolutionary biologists are drawn to groups, such as the spiny-fins, that have apparently undergone explosions in number and form, because they provide opportunities for testing hypotheses about the cause of diversification. One prominent hypothesis in this field is that species richness and morphological evolution increase rapidly when lineages are able to colonize new habitats that have abundant resources and few competitors for the colonizers. This basic mechanism is central to theories of ecological adaptive radiation2.
Mass extinctions — such as that at the end of the Cretaceous, about 65 million years ago — are thought to provide the fortunate surviving lineages with great ecological opportunity by wiping out major players in pre-extinction communities3. One well-known (and well-debated) hypothesis is that a post-Cretaceous radiation of mammal lineages was enabled by the ecological opportunity created by the extinction of non-avian dinosaurs4. Little is known about how the ecological perturbation at the end of the Cretaceous affected fish fauna. Historically, palaeontologists have suggested that fish navigated this transition with little change5, although more recent work reveals that at least some fish communities altered considerably6,7. Friedman1 has used a technique called morphospace analysis to provide compelling evidence that the post-Cretaceous ecological reorganization had a profound influence on the evolution of spiny-fin shape diversity and species richness.
A morphospace (Fig. 1) is a multivariate ordination of possible shapes or forms for organisms. The axes of this space correspond to shape measures (body depth, fin length), so that the physical shape of any organism can be represented by a point in the space, and a group of species, such as the spiny-fins, will form a cloud of points. The size of this cloud, or measures of the dispersion of species in space, indicates the total amount of shape diversity present in the group. Friedman's central finding is that cloud size in spiny-fins is small throughout the Cretaceous but expands strikingly in the early Palaeogene (the time interval immediately following the end-Cretaceous extinction event). Cloud size does not change appreciably over any younger intervals.
Identifying the underlying causes of this shape radiation is difficult: it happened a long time ago, and the fossil record is far from complete. But Friedman1 finds evidence that ecological opportunity was at least partially responsible for the diversification of spiny-fins (Fig. 2). During the Cretaceous, several non-acanthomorph lineages filled the shape-space associated with large, elongate fish-eaters. This entire class of top predators was devastated by the end-Cretaceous extinction. Afterwards, spiny-fins evolved into this region of morphospace, giving rise to some of the top predators of modern oceans, including billfish, barracudas and tuna.
Friedman's analysis1 provides the first quantitative evidence for rapid morphological diversification of spiny-fins during the Palaeogene. But it also raises several questions about the underlying causes. Ecological opportunity created by the extinction of big predatory fishes may account for spiny-fin invasion into one area of shape space, but there are no obvious explanations for the remainder of the post-Cretaceous expansion. Although fishes with powerful bites, including mollusc eaters and grazing herbivores, appear and radiate during the Palaeogene8, Friedman's analysis did not detect a clear signal of morphological change associated with these ecologies. This suggests that body-shape analysis may not be sensitive enough to capture some important aspects of ecological diversification.
Moreover, two lines of evidence potentially complicate the story of spiny-fin diversification. Although, as Friedman shows, skeletal fossils record a strong signal for a post-Cretaceous expansion of spiny-fin shapes, fossil otoliths (hard bones found in the inner ear of fish)9 and time-calibrated molecular phylogenies10 suggest that at least some spiny-fin lineages are much older than their skeletal record. This might mean that Cretaceous and post-Cretaceous levels of spiny-fin diversity were more similar than the skeletal material indicates.
Friedman's study nonetheless shows the potential offered by applying quantitative approaches to the fish fossil record: integration of the steadily proliferating number of fish molecular phylogenies with rigorous treatment of fossil data is the way forward. Such research promises to shake big branches of the fish tree of life and provide ideas to explain the dominant radiation of vertebrates on the planet.
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Proceedings of the National Academy of Sciences (2011)