Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Abstract

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodontidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time-calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.

First timetree of Sphyraenidae (Percomorpha) reveals a Middle Eocene crown age and an Oligo–Miocene radiation of barracudas

“…Interestingly, in spite of the younger ages inferred in our study compared to those of Rabosky et al (2013), most sphyraenid lineages appear to be older than 5 Ma, thus failing to match the pattern observed in many other predominantly reef-associated teleost groups (i.e., Cowman & Bellwood 2011;Frédérich et al 2013;Santini et al 2013c), and to large pelagic predators Santini et al 2013a), all of which experienced significant radiations during the Pliocene and Pleistocene. The differences in the tempo of radiation of these groups were probably linked to a number of environmental factors.…”

“…Much effort has been devoted during the past 10 years to investigate the tempo of diversification of many coral reef-associated fish lineages such as moray eels, snake eels and allies (Reece et al 2010;Santini et al 2013b); pufferfishes, triggerfishes and allies (Alfaro et al 2007;Dornburg et al 2008Dornburg et al , 2011Santini et al 2013cSantini et al , 2013d; wrasses and parrotfishes (Alfaro et al 2009;Cowman et al 2009;Kazancioglu et al 2009); surgeonfishes (Klanten et al 2004;Sorenson et al 2013); butterflyfishes (Cowman & Bellwood 2011); damselfishes (Cowman & Bellwood 2011;Frédérich et al 2013); cardinalfishes (Cowman & Bellwood 2011); and requiem sharks (Sorenson et al 2014). While our understanding of the timing of origin and evolution of reef-associated fish lineages has been greatly increased by these studies, the vast majority of species within these groups tend to be durophagous forms feeding on benthic macroinvertebrates such as crustaceans or shellfish, herbivores or planktivores, with a few lineages having evolved highly specialized diets such as corallivory in butterflyfishes.…”

First molecular timetree of billfishes (Istiophoriformes: Acanthomorpha) shows a Late Miocene radiation of marlins and allies

“…In fact, during the last few years a large number of comparative phylogenetic studies have started to elucidate the tempo and mode of evolution for many lineages of coastal tropical fishes (e.g. Alfaro et al 2007Alfaro et al , 2009Cowman & Bellwood 2011;Dornburg et al 2011;Price et al 2011;Frédérich et al 2013;Santini et al 2013aSantini et al , 2013bSantini et al , 2013cSantini et al , 2013d as well as that of several Antarctic radiations (Rutschman et al 2011;Lautrédou et al 2012), but to date we are aware of only a single published phylogenetic macroevolutionary study of pelagic fishes (Santini et al 2013a). Clearly many more pelagic groups need to be investigated using comparative phylogenetic approaches.…”

Genomic Organization of Repetitive DNAs and Differentiation of an XX/XY Sex Chromosome System in the Amazonian Puffer Fish, <b><i>Colomesus asellus </i></b>(Tetraodontiformes)

“…This genus likely colonized the Amazon region during Pliocene, after marine incursions [Monsch, 1998;Amaral et al, 2013;Santini et al, 2013]. It is considered to be monophyletic [Yamanoue et al, 2011;Amaral et al, 2013;Santini et al, 2013] with species presenting a low mobility and containing venom glands [Oliveira et al, 2006].…”

“…This genus likely colonized the Amazon region during Pliocene, after marine incursions [Monsch, 1998;Amaral et al, 2013;Santini et al, 2013]. It is considered to be monophyletic [Yamanoue et al, 2011;Amaral et al, 2013;Santini et al, 2013] with species presenting a low mobility and containing venom glands [Oliveira et al, 2006]. Three species are currently recognized within this genus: the Amazonian puffer fish, C. asellus [Müller and Troschel, 1849], widely distributed in the Amazon, Orinoco, and Essequibo River basins [Tyler, 1964;Kullander, 2003;Vieira et al, 2013]; the Tocantinensis puffer, C. tocantinensis [Amaral et al, 2013], distributed in the AraguaiaTocantins River basin; and the banded puffer, C. psittacus [Bloch, 1801], which occurs in coastal marine areas.…”