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Acanthemblemaria) ⇑ Ron I Molecular Phylogenetics and Evolution 62 (2012) 159–173 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Reconciling molecules and morphology: Molecular systematics and biogeography of Neotropical blennies (Acanthemblemaria) ⇑ Ron I. Eytan a, , Philip A. Hastings b, Barbara R. Holland c, Michael E. Hellberg a a Department of Biological Sciences, 202 Life Sciences Building, Louisiana State University, Baton Rouge, LA 70803, USA b Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive, La Jolla, CA 92093, USA c School of Mathematics & Physics, University of Tasmania, Private Bag 50, Hobart, TAS 7001, Australia article info abstract Article history: Neotropical reef fish communities are species-poor compared to those of the Indo-West Pacific. An Received 27 June 2011 exception to that pattern is the blenny clade Chaenopsidae, one of only three rocky and coral reef fish Revised 18 September 2011 families largely endemic to the Neotropics. Within the chaenopsids, the genus Acanthemblemaria is the Accepted 19 September 2011 most species-rich and is characterized by elaborate spinous processes on the skull. Here we construct Available online 20 October 2011 a species tree using five nuclear markers and compare the results to those from Bayesian and parsimony phylogenetic analyses of 60 morphological characters. The sequence-based species tree conflicted with Keywords: the morphological phylogenies for Acanthemblemaria, primarily due to the convergence of a suite of Acanthemblemaria characters describing the distribution of spines on the head. However, we were able to resolve some of Chaenopsidae Blennies these conflicts by performing phylogenetic analyses on suites of characters not associated with head Reef fishes spines. By using the species tree as a guide, we used a quantitative method to identify suites of correlated Neotropics morphological characters that, together, produce the distinctive skull phenotypes found in these fishes. A Species trees time calibrated phylogeny with nearly complete taxon sampling provided divergence time estimates that Caribbean recovered a mid-Miocene origin for the genus, with a temporally and geographically complex pattern of Tropical Eastern Pacific speciation both before and after the closure of the Isthmus of Panama. Some sister taxa are broadly sym- Divergence time estimation patric, but many occur in allopatry. The ability to infer the geography of speciation in Acanthemblemaria is Correlated characters complicated by extinctions, incomplete knowledge of their present geographic ranges and by Morphology versus molecules wide-spread taxa that likely represent cryptic species complexes. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction 1.1. Acanthemblemaria Reef communities harbor the greatest marine fish diversity of Acanthemblemaria (Metzelaar, 1919) is the most species-rich any oceanic ecosystem (Sale, 2002). Biodiversity of reef fishes is genus of chaenopsids, as well as one of the most species-rich gen- highest in the Indo-West Pacific and decreases longitudinally to era of Neotropical blennies (Hastings, 2009; Hastings and Springer, the east and west, with the Neotropics being species-poor in com- 2009b). All members in the genus are small (1.2–3.5 cm standard parison (Bellwood and Wainwright, 2002; Briggs, 1974; MacPher- length) and are obligate dwellers of vacated invertebrate holes on son et al., 2009; Mora et al., 2003). A major exception to this shallow (<1–22 m) rocky and coral reefs (Stephens, 1963). As cur- pattern is the Blennioidei, a group of small, bottom-dwelling rocky rently recognized, Acanthemblemaria includes 22 species, 10 in the and coral reef fishes. Blennies are a species-rich group composed of Tropical Eastern Pacific and 12 in the Tropical Western Atlantic six families. Of those, the Labrisomidae, the Dactyloscopidae, and (Hastings, 2009). Since the comprehensive treatment of the family the Chaenopsidae are the only reef fish families entirely or largely Chaenopsidae by Stephens (1963), more named species have been endemic to the New World (Bellwood and Wainwright, 2002; added to Acanthemblemaria than to any other chaenopsid genus. Hastings, 2009). Much of this growth has been due to the recognition that several species with broad distributions contain cryptic, often allopatric taxa (Hastings and Robertson, 1999a; Hastings and Springer, ⇑ Corresponding author. Present address: Yale University, Department of Ecology 2009a,b; Lin and Galland, 2010). and Evolutionary Biology, Environmental Science Center, 21 Sachem Street, #358D, The generic name Acanthemblemaria comes from the Greek New Haven, CT 06520-8106, USA. Akanthos-, or thorn. The name is apt, as Acanthemblemaria blennies E-mail addresses: [email protected] (R.I. Eytan), [email protected] (P.A. Hastings), [email protected] (B.R. Holland), [email protected] (M.E. are typified by the presence of spinous processes on the frontal Hellberg). bones (Metzelaar, 1919; Smith-Vaniz and Palacio, 1974; Stephens, 1055-7903/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2011.09.028 160 R.I. Eytan et al. / Molecular Phylogenetics and Evolution 62 (2012) 159–173 1963). Morphological characters related to head spination repre- a-tropomyosin (atrop). PCR amplification of the full-length rag1 sent the majority of the characters used to infer the interspecific molecule was not possible for some taxa. In these cases, a set of relationships in the group (Hastings, 1990). Recent molecular phy- internal primers were developed for the study and used to amplify logenies of the genus (Eytan, 2010; Lin and Hastings, 2011) recov- rag1. ered Acanthemblemaria as monophyletic, but also recovered Amplicons were purified with a Strataprep PCR Purification Kit conflicts with the morphological hypothesis of Hastings (1990), (Stratagene, La Jolla, CA) or directly sequenced without cleanup in where taxa with clear affinities based on cranial morphology were both directions on an ABI 3100 or 3130 XL automated sequencer not closely related in the molecular phylogeny. with 1/8 reactions of BigDye Terminators (V3.1, Applied Biosys- The characters used for inferring phylogenetic relationships tems) with the amplification primers, or internal primers as indi- must be independent of one another (Kluge, 1989). Suites of mor- cated in Table 1. phological characters that evolve in concert violate this dictate. Such correlated evolution is most likely to occur when a set of 2.3. Sequence alignment and model selection characters underlie a functionally adaptive phenotype or common developmental pathway (Emerson and Hastings, 1998). Such suites Sequences for the four protein-coding genes were aligned of correlated characters can mislead phylogenetic analyses because using MUSCLE (Edgar, 2004) as implemented in Geneious v3.6 they track adaptive history instead of phylogeny (Holland et al., (Drummond et al., 2007). The a-tropomyosin sequences, which 2010; McCracken et al., 1999) or because they are developmentally contained numerous gaps, were aligned in BAli-Phy v2.0.1 (Su- linked to other characters (Schlosser and Wagner, 2004; West- chard and Redelings, 2006) using the GTR substitution model, Eberhard, 2003). In practice, it is difficult to determine the under- gamma distributed rate variation, and the default indel model. lying nature of character correlations. This is because a suite of BAli-Phy was run four times to ensure concordance among runs. characters that are highly correlated with one another are ex- All the samples of the Markov chain taken before convergence, pected to produce the same result as a suite of independent char- as determined by stationarity in the Markov chain, which was acters with good phylogenetic signal: strong support for a given visualized in Tracer v1.5 (Rambaut and Drummond, 2010), were clade (Shaffer et al., 1991). discarded as burnin. The consensus alignment from the run with Here we test whether the homoplastic morphological charac- the highest posterior probability was used for subsequent analy- ters related largely to head spination in Acanthemblemaria are cor- ses and all positions with posterior probabilities less than 0.95 related with one another independent of the phylogeny, and if were discarded. accounting for that correlation can reconcile the molecular and Ten different partitioning strategies were evaluated for both the morphological hypotheses for the genus. We reconstruct the spe- species tree and concatenated analyses. These partitioning strate- cies tree of the genus Acanthemblemaria using five nuclear mark- gies ranged from treating all genes as a single partition, to each ers and employ Bayesian relaxed clock divergence dating to gene and codon position given its own partition (Table 2). Models determine the age of the group and timing of speciation among of sequence evolution for each strategy were determined using the members of the genus. We also examine the historical bioge- jModelTest (Posada, 2008) and the AIC, while partitioning strate- ography of the genus, with the aim of elucidating the geography gies were determined using 2 ln Bayes factors (Kass and Raftery, of speciation in the group. Of particular interest is whether speci- 1995) with the modification of Suchard et al. (2001), implemented ation in this clade has occurred primarily between ocean basins in Tracer v1.5. on either side of the Isthmus of Panama, or within the basins themselves.
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