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Campanella Et Al 2015 Atheri Molecular Phylogenetics and Evolution 86 (2015) 8–23 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Multi-locus fossil-calibrated phylogeny of Atheriniformes (Teleostei, Ovalentaria) Daniela Campanella a, Lily C. Hughes a, Peter J. Unmack b, Devin D. Bloom c, Kyle R. Piller d, ⇑ Guillermo Ortí a, a Department of Biological Sciences, The George Washington University, Washington, DC, USA b Institute for Applied Ecology, University of Canberra, Australia c Department of Biology, Willamette University, Salem, OR, USA d Department of Biological Sciences, Southeastern Louisiana University, Hammond, LA, USA article info abstract Article history: Phylogenetic relationships among families within the order Atheriniformes have been difficult to resolve Received 29 December 2014 on the basis of morphological evidence. Molecular studies so far have been fragmentary and based on a Revised 21 February 2015 small number taxa and loci. In this study, we provide a new phylogenetic hypothesis based on sequence Accepted 2 March 2015 data collected for eight molecular markers for a representative sample of 103 atheriniform species, cover- Available online 10 March 2015 ing 2/3 of the genera in this order. The phylogeny is calibrated with six carefully chosen fossil taxa to pro- vide an explicit timeframe for the diversification of this group. Our results support the subdivision of Keywords: Atheriniformes into two suborders (Atherinopsoidei and Atherinoidei), the nesting of Notocheirinae Silverside fishes within Atherinopsidae, and the monophyly of tribe Menidiini, among others. We propose taxonomic Marine to freshwater transitions Marine dispersal changes for Atherinopsoidei, but a few weakly supported nodes in our phylogeny suggests that further Molecular markers study is necessary to support a revised taxonomy of Atherinoidei. The time-calibrated phylogeny was Molecular clock calibration used to infer ancestral habitat reconstructions to explain the current distribution of marine and fresh- Taxonomy water taxa. Based on these results, the current distribution of Atheriniformes is likely due to widespread marine dispersal along the margins of continents, infrequent trans-oceanic dispersal, and repeated inva- sion of freshwater habitats. This conclusion is supported by post-Gondwanan divergence times among families within the order, and a high probability of a marine ancestral habitat. Ó 2015 Elsevier Inc. All rights reserved. 1. Introduction with adult body sizes ranging from 25 mm to 520 mm in length (Dyer and Chernoff, 1996). Most species are silvery in color with The order Atheriniformes includes about 350 fish species com- a prominent silvery lateral stripe but rainbowfishes (Fam. monly known as silversides, rainbowfishes, and blue eyes, many of Melanotaeniidae) can be very colorful, especially males (Dyer, which are important to support commercial fisheries and the 1998; Dyer and Chernoff, 1996). The most bizarre morphology aquarium trade (Eschmeyer, 2013; Nelson, 2006). They inhabit a among atheriniforms is found in priapium fishes (family wide range of environments from freshwater lakes, lagoons and Phallostethidae), with male phallostethids exhibiting sub-cephalic rivers, to estuaries and coastal marine waters, and are globally dis- copulatory organs derived from modifications of the pelvic skele- tributed in tropical and temperate regions (Table 1). Some ton (Parenti, 1986). atheriniform species are exclusively marine, but many others are The monophyly of Atheriniformes is supported by ten morpho- restricted to freshwater (Nelson, 2006) and some diadromous logical synapomorphies (Dyer and Chernoff, 1996). Monophyly species undertake seasonal migrations between marine and fresh- also is supported by molecular analyses of mitogenomes for a water habitats (Dyer and Chernoff, 1996). Many atheriniforms small number of taxa (Setiamarga et al., 2008), by analyses of cyto- exhibit a wide range of salinity tolerance typical of euryhaline chrome b and RAG-1 data for 47 ingroup taxa (Bloom et al., 2012), species. The order is moderately diverse in terms of morphology, but not by a parsimony analysis combining morphology, mitochondrial, and nuclear gene data (Sparks and Smith, 2004). A recent molecular phylogenetic study of 1416 ray-finned fishes ⇑ Corresponding author at: Department of Biological Sciences, The George based on 21 gene fragments that included 25 atheriniform taxa Washington University, 2023 G St. NW, Washington, DC 20052, USA. from 8 of the 11 recognized families also resolved the monophyly E-mail address: [email protected] (G. Ortí). http://dx.doi.org/10.1016/j.ympev.2015.03.001 1055-7903/Ó 2015 Elsevier Inc. All rights reserved. D. Campanella et al. / Molecular Phylogenetics and Evolution 86 (2015) 8–23 9 Table 1 Families of Atheriniformes according to Nelson (2006) and Eschmeyer and Fong (2014), valid genera, their geographic distribution, habitat type, and alternative taxonomic arrangements. Family and Geographic distribution and Included genera Taxonomic observations common name habitat Atherinidae Old Indo-West Pacific and Alepidomus, Atherina, Atherinason, Atherinomorus, Number of subfamilies included varies between World Atlantic; freshwater, marine, BleheratherinaA, Craterocephalus, HypoatherinaA, twoa,b, threec, sixd, and ninee; 12 genera with 68 Silversides and brackish Kestratherina, Leptatherina, SashatherinaA, StenatherinaA, species TeramulusA Atherinopsidae North, Central, and South Atherinella, Atherinops, Atherinopsis, Basilichthys, Formerly a subfamily in Atherinidaea,d,e, later New World America (Atlantic and Pacific); Chirostoma, ColpichthysA, Labidesthes, Leuresthes, recognized as a familyb; includes two subfamilies Silversides freshwater, marine, and Melanorhinus, Membras, Menidia, Odontesthes, Poblana (Atherinopsinae and Menidiinae); 13 genera with 109 brackish species Atherionidae Indian Ocean and Western Atherion Previously a subfamily of Atherinidaee,f, later elevated Pricklenose Pacific; marine to familyc,g; 1 genus with three species silversides Bedotiidae Central and eastern Bedotia, Rheocles Previously a subfamily of Melanotaeniidaec, later Madagascar Madagascar; freshwater elevated to familyh; 2 genera with 16 species rainbowfishes Dentatherinidae Tropical western Pacific; Dentatherina merceriA Formerly a subfamily of Atherinidae, a subfamily of Tusked marine Phallostethidaei, or as a separate familyj; monotypic silversides Isonidae Surf Indo-West Pacific; marine Iso Either within Notocheiridaec, or as its own familyb,k; silversides five species Melanotaeniidae Australia, New Guinea, eastern Cairnsichthys, Chilatherina, Glossolepis, Iriatherina, Also as a subfamily within Melanotaeniidaec;seven Rainbowfishes Indonesia; freshwater, few Melanotaenia, PelangiaA, Rhadinocentrus genera with 80 species brackish, rarely marine Notocheiridae Southern South America; Notocheirus hubbsi Also as a subfamily in Atherinopsidaek, sister to Surf silversides marine Atherinopsidaeg, or with Iso in a monophyletic familyc; monotypic Phallostethidae Southeast Asia (Philippines to GulaphallusA, Neostethus, PhallostethusA, PhenacostethusA Proposed as a subfamily within Phallostethidae, sister Priapium fishes Thailand and Sumatra); to Dentatherininaec,g; 4 genera with 23 species freshwater and brackish Pseudomugilidae Australia and New Guinea; Kiunga, Pseudomugil, PopondichthysA, ScaturiginichthysA Formerly a subfamily within Melanotaeniidaec;4 Blue eyes freshwater and brackish, rare genera with 18 species marine Telmatherinidae Sulawesi, Misool and Batanta Kalyptatherina, Marosatherina, ParatherinaA, Formerly a subfamily within Melanotaeniidaec;5 Sailfin Island; freshwater TelmatherinaA, TominangaA genera with 18 species silversides a Fowler (1903). b Saeed et al. (1994). c Dyer and Chernoff (1996). d Jordan and Hubbs (1919). e Schultz (1948). f Patten (1978). g Aarn and Ivantsoff (1997). h Stiassny et al. (2002). i Parenti (1984). j Parenti and Louie (1998). k Bloom et al. (2012). A Genera not sampled in this study. of this order with high bootstrap support (Betancur et al., 2013). In Atherinopsidae (suborder Atherinopsoidei) as the sister-group to that study, Atheriniformes was resolved within the same clade the remaining families (Fig. 1A, B, D, E, F). Within (superorder Atherinomorphae) as Beloniformes and Atherinopsoidei, recent molecular analyses (Bloom et al., 2012) Cyprinodontiformes, in agreement with previous hypotheses supported previous hypotheses by Saeed et al. (1994) and Aarn (Parenti, 1993). and Ivantsoff (1997) regarding the composition of the family The number of atheriniform families and their composition Notocheiridae (‘‘surf silversides’’). These authors placed have been relatively variable over time (Nelson, 2006). A summary Notocheirus hubbsi, the surf silverside from temperate coastal of current hypotheses is presented in Table 1. Interrelationships of waters of Argentina and Chile, closer to or nested within the family Atheriniformes have been examined by several authors based on Atherinopsidae (Fig. 1B and D). A second genus of surf silversides morphological characters (Aarn and Ivantsoff, 1997; Dyer and (Iso, with five Indo-Pacific species) traditionally included in the Chernoff, 1996; Ivantsoff et al., 1987; Parenti, 1984, 1993; Rosen, family Notocheiridae was shown to be distantly related and 1964; Rosen and Parenti, 1981; White et al., 1984) and DNA assigned to Isonidae, suggesting that many of the morphological sequence data (Betancur
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