Cleaners among wrasses: Phylogenetics and evolutionary patterns of cleaning behavior within Labridae q Vikram B. Baliga ⇑ , Chris J. Law Department of Ecology and Evolutionary Biology, Long Marine Laboratory, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, CA 95060, USA article info Article history: Received 11 July 2015 Revised 5 September 2015 Accepted 8 September 2015 Available online 13 October 2015 Keywords: Cleaner fishes Labridae Phylogeny Stochastic character mapping abstract Cleaner fishes remove and consume ectoparasites and are often categorized by whether they perform this behavior: (1) predominately as juveniles, (2) facultatively throughout ontogeny, or (3) obligately. Through a literature search, we confirmed that with at least 58 species exhibiting cleaning behavior, the Labridae (wrasses, parrotfishes, and allies) contain the highest diversity of cleaner fishes. In fact, there are 3–4 times as many cleaners within labrids as there are in any other marine group. The distribution and underlying causes of this exceptional diversity have not been determined. Here, we assess the topological and temporal patterns of labrid cleaner evolution. We used maximum likelihood and Bayesian approaches to infer the phylogenetic relationships and divergence times between 320 labrid species (50.7% of nominal species). We then employed stochastic character mapping to infer how and when cleaning behavior evolved. We estimate that cleaning has independently evolved 26–30 times in the Labridae, and all such events likely occurred no earlier than in the late Miocene. Given the current sampling and pattern of transitions, we hypothesize that the majority of facultative or obligate cleaning may have evolved through heterochrony. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction The Labridae (wrasses, parrotfishes, and hogfishes) is a speciose group of marine perciform fishes that occupies diverse ocean habitats worldwide. Labrids are well known for being some of the most common and functionally important inhabitants of coral reef ecosystems, revealing tremendous diversity in morphology and trophic strategies (Wainwright et al., 2004; Bellwood et al., 2006; Price et al., 2011). Labrids feature, among myriad trophic strategies, extreme specializations such as corallivory, planktivory, and molluscivory. One of the most fascinating specializations within the Labridae is cleaning behavior. Cleaner fishes are taxa that remove and consume ectoparasites off other organisms. The evolution of clean- ing behavior presents one of the few examples of mutualisms among vertebrates (Bronstein, 1994; Poulin and Grutter, 1996). While cleaners typically clean other fishes, they have also been observed to inspect a variety of marine vertebrates and inverte- brates (see Grutter, 2010 for a review of cleaner fish behaviors). The presence of cleaners in a habitat can have tremendous ecological consequences. For instance, experimental removal of the bluestreak cleaner wrasse (Labroides dimidiatus) has been shown to affect the behavior, recruitment dynamics, and sizes of client fishes (Waldie et al., 2011). Cleaning is not exclusive to labrids; in fact, at least 18 marine families of fishes include at least one member that cleans. Coté (2000) provides an extensive list of cleaner fishes. According to Coté (2000), 50 species of labrids are documented as cleaners. This is three times as many species as in the next highest group the Gobiidae, within which 14 species of cleaners are recognized. This suggests cleaner fish species richness is not directly proportional to clade diversity, especially when considering the Gobiidae has close to 2000 extant members. Furthermore, of the various groups of marine fishes in which cleaning is found, the overwhelming major- ity contain five or fewer species that clean (Coté, 2000). These met- rics underscore the exceptional diversity of labrid cleaners, marking labrids as a model clade within which to explore the evolution of cleaning. Cleaner fishes can be categorized by whether they perform the behavior (1) predominately as juveniles, (2) facultatively through- out ontogeny, or (3) obligately (Coté, 2000). Obligate cleaners are more conspicuous and most of what is known about cleaning behavior has been determined through observing species in the obligate cleaner genus Labroides. For example, L. dimidiatus http://dx.doi.org/10.1016/j.ympev.2015.09.006 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. q This paper was edited by the Associate Editor Giacomo Bernardi. ⇑ Corresponding author at: Center for Ocean Health, Long Marine Laboratory, 100 Shaffer Road, Santa Cruz, CA 95060, USA. E-mail address: vbaliga@ucsc.edu (V.B. Baliga). Molecular Phylogenetics and Evolution 94 (2016) 424–435 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev