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Adaptive Radiation in Labrid Fishes

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Adaptive Radiation in Labrid Fishes ORIGINAL ARTICLE doi:10.1111/evo.13670 Adaptive radiation in labrid fishes: A central role for functional innovations during 65 My of relentless diversification Edward D. Burress1,2 and Peter C. Wainwright1 1Department of Evolution and Ecology, Center for Population Biology, University of California, Davis, California 95616 2E-mail: [email protected] Received June 26, 2018 Accepted December 11, 2018 Early burst patterns of diversification have become closely linked with concepts of adaptive radiation, reflecting interest in the role of ecological opportunity in modulating diversification. But, this model has not been widely explored on coral reefs, where biodiversity is exceptional, but many lineages have high dispersal capabilities and a pan-tropical distribution. We analyze adaptive radiation in labrid fishes, arguably the most ecologically dominant and diverse radiation of fishes on coral reefs. We test for time- dependent speciation, trophic diversification, and origination of 15 functional innovations, and early bursts in a series of functional morphological traits associated with feeding and locomotion. We find no evidence of time-dependent or early burst evolution. Instead, the pace of speciation, ecological diversification, and trait evolution has been relatively constant. The origination of functional innovations has slowed over time, although few arose early. The labrid radiation seems to have occurred in response to extensive and still increasing ecological opportunity, but within a rich community of antagonists that may have prevented abrupt diversification. Labrid diversification is closely tied to a series of substantial functional innovations that individually broadened ecological diversity, ultimately allowing them to invade virtually every trophic niche held by fishes on coral reefs. KEY WORDS: Early burst, ecological opportunity, functional innovation, rates of evolution, trophic diversity. Adaptive radiation–the rapid diversification of a lineage into of diversification (Glor 2010; Yoder et al. 2010; Stroud and Losos novel distinct adaptive zones (Simpson 1953)–holds a special 2016). position in our understanding of the origins of biological diver- In recent years, the so-called “early burst” has flirted with be- sity. Adaptive radiation links population dynamics, competition, coming synonymous with adaptive radiation. Many studies now ecological opportunity, and the fitness landscape with specia- “test for adaptive radiation” by looking for evidence of an early tion and interesting macroevolutionary outcomes (Schluter 2000; burst of phenotypic diversification or speciation in their study Mayr 2001). Although not universally agreed to be a necessary group. Indeed, some well-known examples of adaptive radiation component, theory (Simpson 1953; Schluter 2000; Gavrilets and exhibit high rates of morphological or ecological differentiation Losos 2009) and empirical work (Losos et al. 2001; Rabosky early in the radiation (Harmon et al. 2003, 2008; Freckelton and 2009; Martin and Wainwright 2013) have led to the realization Harvey 2006; Agrawal et al. 2009; Mahler et al. 2010). Similarly, a that adaptive radiation is often characterized by an early period declining rate of lineage diversification from the earliest stages of of rapid speciation and ecological diversification that slows as the radiation toward the present has been interpreted as evidence ecological opportunity is exploited and niches are filled (of- of parallel reductions in ecological opportunity in the context of ten referred to as an “early burst”). Thus, for many authors adaptive radiation (Rabosky and Lovette 2008; Rabosky 2009; adaptive radiation requires the rapid diversification of a single Glor 2010). But, whether diversity-dependent species diversifi- lineage into many, ecologically diverse species (Schluter 2000; cation and early bursts of trait evolution should be equated with Simpson 1953), a view that places heavy weight on the impor- adaptive radiation is challenged by the many radiations that do not tance of changes in ecological opportunity in modulating the pace show such patterns (Harmon et al. 2010; Derryberry et al. 2011; C 2018 The Author(s). Evolution C 2018 The Society for the Study of Evolution. 1 Evolution E. D. BURRESS AND P. C. WAINWRIGHT Puttick 2018), highlighting a need for a nuanced concept of adap- 15 functional innovations associated with niche-shifts in feeding tive radiation that considers the diversity of circumstances and habits and habitat use. Cumulatively, these tests are used to de- mechanisms under which adaptive radiation takes place (Gavrilets termine whether labrid fishes fit the classic notion of an adaptive and Losos 2009). radiation in which diversification slows over time as the clade Coral reefs harbor exceptional biodiversity, including about becomes more diverse and fills available niches (Simpson 1953; 20% of all fish species (Kulbicki et al. 2013). Among more than Schluter 2000; Stroud and Losos 2016). 70 families of coral reef fishes, Labridae (wrasses and parrot- fishes) stands out as consistently ranking among the most species- rich, locally abundant, ecologically diverse, and central to ecosys- Methods tem processes (Bellwood 1996; Robertson 1998; Bellwood and PHYLOGENETIC INFERENCE Wainwright 2002). Over 510 labrid species occur on coral reefs We used a previously published phylogeny of 320 labrid species throughout the tropics, making them the most species-rich fish (Baliga and Law 2016), representing slightly more than half of family found on coral reefs, with another 100 species found the nominal species (Froese and Pauly 2015). Briefly, their dataset in temperate rocky habitats around the world (Cowman 2014). included four mitochondrial (12S, 16S, COI, and Cyt b) and three Species range in body size from the tiny 5 cm Wetmorella tanakai nuclear gene regions (RAG2, TMO4c4, and S7), with 5462 total to the giant 230 cm, 190 kg Cheilinus undulatus. Their trophic base pairs obtained from GenBank. Sequences were aligned in diversity covers nearly the entire range of feeding habits found Geneious 4.8.5 (Kearse et al. 2012), the best-fitting model of nu- among fishes on coral reefs, including myriad crustaceans, mol- cleotide substitution was identified using jModelTest 2.0 (Darriba luscs, echinoderms, zooplankton, fishes, polychaetes, bryozoans et al. 2012), and sequences were concatenated into a supermatrix and in some of the more specialized taxa, algae, detritus, au- using SequenceMatrix 1.7.8 (Vaidya et al. 2011). Then, the au- totrophic microbes, foraminifera, coral mucus, and ectoparasites thors estimated phylogenetic trees using a relaxed log normal of other fishes. Their feeding activities can have profound effects clock model with BEAST 2.2.1 (Bouckaert et al. 2014) under a on benthic communities, especially parrotfishes, which constantly GTR + model. Seven informative parametric priors based on graze hard surfaces, shaping recruitment of algae, clearing space fossil and biogeographic information were set during this proce- for other settlers (Burkepile and Hay 2008; Bonaldo et al. 2014), dure (Baliga and Law 2016). The authors ran five separate MCMC and acting as the most potent bioeroders of carbonate reef struc- runs and after discarding burn-in (15–20%), the combined set tures (Bellwood 1995; Bruggemann et al. 1996). Labrid diversity of runs included 41,323 trees, which were used to estimate the extends along other dimensions as well, including depth (Wain- maximum clade credibility (MCC) tree in TreeAnnotator 2.2.1 wright et al. 2018), microhabitat (Bellwood and Wainwright 2001; (Bouckaert et al. 2014; Fig. S1). In this study, to account for un- Fulton et al. 2005), a wide range of mating systems (Robertson certainty in phylogenetic tree topology and divergence times, we and Choat 1974; Warner 1984), and variation in patterns of sexual repeated most analyses across 1000 trees sampled randomly from ontogeny (Warner and Robertson 1978) that have led to extensive the posterior distribution (see below for analysis-specific details). color diversity. With their high species richness, local abundance, and ecological exuberance, labrids are the quintessential adaptive LINEAGE DIVERSIFICATION radiation of fishes on coral reefs. But are they? We employed the γ test using the R package PHYTOOLS (Revell In the present study, we evaluate the tempo of the labrid 2012) to evaluate the pace of diversification through time. We adaptive radiation, specifically asking whether they exhibit early estimated γ for each of the 1000 randomly sampled trees from the bursts of speciation, trait evolution and ecology, consistent with an posterior distribution, then employed the Monte Carlo Constant abrupt response to ecological opportunity. Using a time-calibrated rates test (MCCR) implemented in LASER (Rabosky 2006a) to molecular phylogeny, we test for changes in net diversification rate conduct γ-statistic analysis for incompletely sampled phyloge- through the 65 My history of the group. We reconstruct the his- nies (Pybus and Harvey 2000). Complete phylogenies (i.e., with tory of feeding habits in labrids, asking whether we see evidence 638 tips) were simulated under the null hypothesis of a constant of diversity-dependent dietary diversification. We also test for an pure birth diversification process and taxa were randomly pruned early burst in the evolution of several continuous functional traits to mimic the degree of incomplete taxon sampling in the empiri- that characterize the complex labrid feeding
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