Diversity and Disparity Through Time in the Adaptive Radiation of Antarctic Notothenioid Fishes
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doi: 10.1111/jeb.12570 Diversity and disparity through time in the adaptive radiation of Antarctic notothenioid fishes M. COLOMBO*, M. DAMERAU†,R.HANEL†,W.SALZBURGER*‡ & M. MATSCHINER*‡ *Zoological Institute, University of Basel, Basel, Switzerland †Thunen€ Institute of Fisheries Ecology, Hamburg, Germany ‡Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, Oslo, Norway Keywords: Abstract adaptive radiation; According to theory, adaptive radiation is triggered by ecological opportunity early burst; that can arise through the colonization of new habitats, the extinction of geometric morphometrics; antagonists or the origin of key innovations. In the course of an adaptive incomplete lineage sorting; radiation, diversification and morphological evolution are expected to slow species tree. down after an initial phase of rapid adaptation to vacant ecological niches, followed by speciation. Such ‘early bursts’ of diversification are thought to occur because niche space becomes increasingly filled over time. The diver- sification of Antarctic notothenioid fishes into over 120 species has become one of the prime examples of adaptive radiation in the marine realm and has likely been triggered by an evolutionary key innovation in the form of the emergence of antifreeze glycoproteins. Here, we test, using a novel time-calibrated phylogeny of 49 species and five traits that characterize not- othenioid body size and shape as well as buoyancy adaptations and habitat preferences, whether the notothenioid adaptive radiation is compatible with an early burst scenario. Extensive Bayesian model comparison shows that phylogenetic age estimates are highly dependent on model choice and that models with unlinked gene trees are generally better supported and result in younger age estimates. We find strong evidence for elevated diversifica- tion rates in Antarctic notothenioids compared to outgroups, yet no sign of rate heterogeneity in the course of the radiation, except that the nototheni- oid family Artedidraconidae appears to show secondarily elevated diversifi- cation rates. We further observe an early burst in trophic morphology, suggesting that the notothenioid radiation proceeds in stages similar to other prominent examples of adaptive radiation. extinction of antagonists or the emergence of evolu- Introduction tionary key innovations that allow the invasion of new Adaptive radiation, that is the evolution of a multitude adaptive zones (Heard & Hauser, 1995; Schluter, 2000; of species as a consequence of the adaptation to new Yoder et al., 2010). Starting from a single ancestor, ecological niches, is considered to be responsible for adaptively radiating groups are expected to differentiate much of the diversity of life on Earth (Simpson, 1953; into an array of morphologically and ecologically Schluter, 2000). In general, adaptive radiation is diverse species filling multiple available ecological thought to result from ecological opportunity in the niches. Mathematical models of adaptive radiation form of vacant ecological niches that may have become predict that rates of diversification and morphological available due to the colonization of new habitats, the evolution are inversely correlated with available niche space, thus leading to a slowdown in diversification rates as niche space becomes increasingly filled (Gavri- Correspondence: Walter Salzburger and Michael Matschiner, Zoological lets & Vose, 2005; Gavrilets & Losos, 2009). As a result, Institute, University of Basel, Vesalgasse 1, Basel 4051, Switzerland. Tel.: +41 61 267 03 03; fax: +41 61 267 03 01; e-mails: walter. both speciation events and morphological change [email protected] and [email protected] would be concentrated in an ‘early burst’ near the ª 2014 THE AUTHORS. J. EVOL. BIOL. 28 (2015) 376–394 376 JOURNAL OF EVOLUTIONARY BIOLOGY PUBLISHED BY JOHN WILEY & SONS LTD ON BEHALF OF EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY. THIS IS AN OPEN ACCESS ARTICLE UNDER THE TERMS OF THE CREATIVE COMMONS ATTRIBUTION LICENSE, WHICH PERMITS USE, DISTRIBUTION AND REPRODUCTION IN ANY MEDIUM, PROVIDED THE ORIGINAL WORK IS PROPERLY CITED. Diversity and disparity in adaptive radiation 377 beginning of the history of an adaptive radiation (Simp- Notothenioids dominate the waters surrounding the son, 1953; Erwin, 1994; Losos & Miles, 2002). Antarctic continent both by species number (47%) and Temporally declining rates of speciation are often by biomass (90–95%) (Eastman, 2005) and evolved observed in molecular phylogenies of radiating clades, exceptional adaptations in response to an environment including Anolis lizards of the Caribbean islands (Rabo- that is shaped by subzero water temperatures and the sky & Glor, 2010), North American wood warblers widespread presence of sea ice. A common characteristic (Rabosky & Lovette, 2008), squamates (Burbrink et al., of all notothenioids is the lack of a swim bladder. There- 2012), Neotropical cichlid fishes (Lopez-Fern andez fore, most notothenioid species are negatively buoyant. et al., 2013) and bats (Yu et al., 2014). In addition, To compensate for this morphological limitation, several inverse relationships between radiation age and species notothenioid clades evolved adaptations to regain neu- counts have been found in the replicate adaptive radia- tral buoyancy and are able to utilize (in addition to the tions of Tetragnatha spiders on the Hawaiian islands ancestral benthic habitat) a set of different environments (Gillespie, 2004), and in those of cichlid fishes in East such as semipelagic, epibenthic, cryopelagic or pelagic African Rift lakes (Seehausen, 2006). This suggests that habitats (Eastman, 2005). Morphological adaptations to not only speciation rates, but also the total number of enable the exploitation of these habitats include reduced species can decline subsequently to an early burst, a mineralization of the skeleton and deposition of lipids in phenomenon termed ‘overshooting’ (Gavrilets & Losos, adipose cells (Balushkin, 2000; Eastman, 2000). These 2009). adaptations, probably together with diversification in However, most empirical support for early bursts in body and head shape, enabled notothenioids to feed on morphological disparity derives from paleontological a diverse diet. Stomach content analyses reveal a diet studies, which show that fossil groups often obtain consisting of fish, krill and mysids for some species as maximum disparity early in their history, followed by well as polychaetes, ophiuroids and echinoderms for subsequent decline (Foote, 1997). Several methods others (Rutschmann et al., 2011). have been developed to infer early bursts in disparity It is thought that the adaptive radiation of nototheni- from extant species on the basis of phylogenetic analy- oids followed ecological opportunity after the drop to ses (Harmon et al., 2003, 2010; Slater & Pennell, 2014). subzero water temperatures around Antarctica that pre- In practice, however, these methods often fail to detect sumably led to the extinction of most of the previously early bursts in morphological diversification in even the existing ichthyofauna in the Late Oligocene or Early most prominent examples of adaptive radiation (Har- Miocene (Eastman, 1993; Near, 2004; Matschiner et al., mon et al., 2010; but see Mahler et al., 2010; Slater 2011). Due to the emergence of antifreeze glycoproteins et al., 2010; Lopez-Fern andez et al., 2013). (AFGPs) in the ancestor of five predominantly Antarctic Adaptive radiation has also been proposed to progress notothenioid families (the ‘Antarctic clade’) (Chen et al., in stages in the sense that diversification occurs along 1997; Cheng et al., 2003), notothenioids of this particu- different axes at different intervals of a radiation (Stre- larly species-rich group were able to survive in subzero elman & Danley, 2003; Ackerly et al., 2006; Gavrilets & waters and could effectively exploit ecological niches Losos, 2009). Verbal models, as well as a mathematical that had become vacant. Thus, AFGPs may have acted as theory of speciation (Gavrilets, 2004), predict that a key innovation, triggering the adaptive radiation of the diversification would (i) be driven by divergence notothenioid Antarctic clade (Matschiner et al., 2011), according to macrohabitat, followed by (ii) increasing possibly facilitated by standing genetic variation (Braw- divergence with respect to microhabitat, (iii) traits that and et al., 2014). However, a recent phylogenetic study control both for local adaptation and nonrandom mat- (Near et al., 2012) found that major pulses of lineage ing and (iv) traits that control for survival and repro- diversification occurred substantially later than the evo- duction. However, the order of stages seems to depend lution of AFGPs, which implies that other drivers were on diverse factors that differ between adaptive radia- more important in driving diversification and acted at tions. For example, Phylloscopus leaf warblers apparently later stages. Thus, the timing and trigger of the notothe- diverged in the order of body size, foraging morphol- nioid adaptive radiation remains a matter of debate. ogy/behaviour and then habitat (Richman, 1996), and Although the diversification of notothenioids has trophic morphology has been suggested to diversify been the subject of a large number of recent investiga- before macrohabitat adaptations in cichlids from Lake tions (Near & Cheng, 2008; Rutschmann et al., 2011; Tanganyika (Muschick et al., 2014). In contrast, Lake Near