Accepted Manuscript A multi-gene dataset reveals a tropical New World origin and Early Miocene diversification of croakers (Perciformes: Sciaenidae) Pei-Chun Lo, Shu-Hui Liu, Ning Labbish Chao, Francis K.E. Nunoo, Hin-Kiu Mok, Wei-Jen Chen PII: DOI: Reference:

S1055-7903(15)00094-9 http://dx.doi.org/10.1016/j.ympev.2015.03.025 YMPEV 5157

To appear in:

Molecular Phylogenetics and Evolution

Received Date: Revised Date: Accepted Date:

5 February 2015 26 March 2015 28 March 2015

Please cite this article as: Lo, P-C., Liu, S-H., Chao, N.L., Nunoo, F.K.E., Mok, H-K., Chen, W-J., A multi-gene dataset reveals a tropical New World origin and Early Miocene diversification of croakers (Perciformes: Sciaenidae), Molecular Phylogenetics and Evolution (2015), doi: http://dx.doi.org/10.1016/j.ympev.2015.03.025

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A multi-gene dataset reveals a tropical New World origin and Early Miocene

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diversification of croakers (Perciformes: Sciaenidae)

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Original Research Article

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Pei-Chun Loa, Shu-Hui Liu a, Ning Labbish Chao b, Francis K. E. Nunooc, Hin-Kiu

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Mokd and Wei-Jen Chena*

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a

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Taipei 10617, Taiwan

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b

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Pingtung, 94450, Taiwan

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c

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Boundary, Accra, Ghana

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d

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Road, Kaohsiung 80424, Taiwan

Institute of Oceanography, National Taiwan University, No.1, Sec. 4 Roosevelt Road

National Museum of Marine Biology & Aquarium, No.2, Houwan Road, Checheng,

Department of Marine and Fisheries Sciences, University of Ghana, Legon

Department of oceanography, National Sun Yat-Sen University, No.70, Lienhai

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* Corresponding author Wei-Jen Chen Room 301, Institute of Oceanography, National Taiwan University, No.1, Sec. 4

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Roosevelt Road Taipei 10617, Taiwan Phone number: +886 2 33661630

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Fax number: +886 2 23637062 E-mail address: [email protected]

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ABSTRACT

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Widely distributed groups of living animals, such as the predominantly marine fish

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family Sciaenidae, have always attracted the attention of biogeographers to document

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the origins and patterns of diversification in time and space. In this study, the

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historical biogeography of the global Sciaenidae is reconstructed within a molecular

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phylogenetic framework to investigate their origin and to test the hypotheses

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explaining the present-day biogeographic patterns. Our data matrix comprises six

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mitochondrial and nuclear genes in 93 globally sampled sciaenid species from 52

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genera. Within the inferred phylogenetic tree of the Sciaenidae, we identify 15 main

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and well-supported lineages; some of which have not been recognized previously.

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Reconstruction of habitat preferences shows repeated habitat transitions between

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marine and euryhaline environments. This implies that sciaenids can easily adapt to

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some variations in salinity, possibly as the consequence of their nearshore habitats and

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migratory life history. Conversely, complete marine/euryhaline to freshwater

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transitions occurred only three times, in South America, North America and South

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Asia. Ancestral range reconstruction analysis concomitant with fossil evidence

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indicates that sciaenids first originated and diversified in the tropical America during

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the Oligocene to Early Miocene before undergoing two range expansions, the first to

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Eastern Atlantic and the secondly to the Indo-West Pacific where a maximum species

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richness is observed. The uncommon biogeographic pattern identified is discussed in

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relation to current knowledge on origin of gradients of marine biodiversity towards

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the center of origin hypothesis in the Indo-West Pacific.

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Keywords Biogeography; Indo-West Pacific; New World, Sciaenidae; Systematics;

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Time-calibrated phylogeny

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1. Introduction

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Sciaenids are commonly called croakers or drums because of their propensity to

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produce sounds using sonic muscles and swim bladder (Tower, 1908; Ramcharitar et

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al., 2006). These sounds might be species- or sex- specific and are used for

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communication (Mok and Gilmore, 1983; Myrberg Jr, 1997; Amorim and Hawkins,

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2000; Ladich, 2004;Gannon, 2007; Kasumyan, 2009; Mok et al., 2009). This

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particular feature makes sciaenids attractive models for acoustic-related research

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focusing on the behaviors, mate choice, and evolution (Connaughton et al., 2000;

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Gannon, 2007; Aalbers, 2008). In spite of their attractive acoustic behavior, the

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taxonomy, biogeography, and evolutionary relationships among the species remain

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largely uncertain, primarily due to absence of a comprehensive phylogeny for

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sciaenids.

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Sciaenids form one of the largest families of the Perciformes, comprising 66

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genera and approximately 291 species (Eschmeyer and Fong, 2013). Anatomical

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examination supports its monophyly but does not identify its sister group (Sasaki,

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1989). Current advances on molecular phylogenetics of the Percomorpha do not

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resolve the sister group of Sciaenidae but circumscribe a restrictive list of possibilities

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within the clade N sensu Chen et al. (2007). This clade includes also some of the

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major groups of tropical fishes inhabiting coral reefs (e.g., Chaetodontidae,

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Lethrinidae, Tetraodontiformes) and blackish water (e.g., Haemulidae), as well as

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major temperate water lineages (e.g., Moronidae, Sparidae), and deep-sea taxa (e.g.,

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Lophiiformes) (Chen et al., 2007; Betancur-R et al., 2013; Near et al., 2013; W.-J.

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Chen, et al., 2014a).

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Chao (1978) first assessed the phylogenetic relationships of all western Atlantic

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sciaenids and placed them into 11 generic groups based on their swim bladder,

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otoliths and external morphology. The most comprehensive revision for the

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systematics of the Sciaenidae was made by Sasaki (1989) who proposed a new

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phylogenetic hypothesis based on a cladistic analysis of several osteological and

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myological characters and a large taxonomic sampling with 87 species (from 60

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genera) distributed worldwide. Accordingly, Sasaki (1989) revised the classification of

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Sciaenidae by dividing the family into four synapomorphy-based subgroups: I, II, III

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and IV (Appendix A), yet the relationships among the subgroups and within the

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subgroups remain mostly unresolved.

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All previous molecular phylogenetic studies of the Sciaenidae were limited to

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few taxa, a particular geographical region, and only mitochondrial markers were used

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to infer the relationships (Vinson et al., 2004; Vergara-Chen et al., 2009; Cooke et al.,

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2012; Santos et al., 2013; Barbosa et al., 2014). Due to their limited taxonomic

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samplings, none of these molecular studies provided a general test of Sasaki’s (1989)

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hypothesis and others that allow a better understanding of evolution of the global

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Sciaenidae, for instance, the historical hypotheses explaining their current distribution

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patterns.

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Sciaenids are distributed worldwide in coastal zones of tropical and temperate

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regions (Chao, 1978, 1986; Sasaki, 1989). Most of the species are marine. A few

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species (euryhaline) are able to adapt to a wide range of salinities. However, only

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about 25 species in six genera strictly inhabit freshwaters in North America (one

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species), South America (23 species) and Southeast Asia (one species) (Casatti, 2002).

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The distribution of Sciaenidae and their species diversity pattern across the oceanic

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regions are summarized in Figure 1. Widely distributed groups of living animals, such 4

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as the family Sciaenidae, have always attracted the attention of biogeographers to

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document the origins and patterns of diversification in time and space. In fact, the

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historical factors and processes leading to the present-day biogeographic patterns have

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already been studied in some of the important fish groups such as Clupeoidei

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(sardines and anchovies) (Lavoué et al., 2013), Otophysi (including major freshwater

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water lineages of the teleost fishes) (Chen et al., 2013), Percichthyoidea (temperate

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freshwater perch-like fishes) (W.-J. Chen et al., 2014b), and Tetraodontidae

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(pufferfishes) (Yamanoue et al., 2011; Santini et al., 2013b), yet there are with no

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conclusive hypothesis proposed for the highly diverse Sciaenidae.

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Sasaki (1989) was the first to concretely discuss the historical biogeography and

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evolutionary origin of the Sciaenidae using his phylogenetic results. Three alternative

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hypotheses were considered: 1- the ancestor of Sciaenidae was distributed worldwide

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with subsequent diversification predominantly occurring via vicariant events; 2- New

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World origin of the ancestor with eastward and/or westward dispersal (favored

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hypothesis of Sasaki); 3- Old World origin of the ancestor with eastward and/or

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westward dispersal. Because of a general lack of phylogenetic resolution among the

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main groups of sciaenids, it was difficult to objectively choose the best

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biogeographical hypothesis for this group. Despite the fact that fossil records might be

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indicative for studying the historical biogeography, Sasaki (1989) did not consider

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fossil data in his analysis.

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Regarding the species diversity pattern, the sciaenid species richness amongst

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regions, is somewhat atypical as it is not strongly unbalanced (Fig. 1A) as it can be

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observed in several other groups of fishes and other marine animals. Typically, the

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Indo-West Pacific region comprises more species than any other regions in most of

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the worldwide-distributed marine groups (Tittensor et al., 2010). In sciaenids, the

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respective numbers of species in the Indo-West Pacific, Eastern Pacific and Western 5

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Atlantic regions are comparable with about 82 to 93 species per region. It is

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sometimes assumed that the region of maximal diversity is also the region of origin of

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a group of organisms (Briggs, 1999, 2003; Orrell et al., 2002; Santini and

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Winterbottom, 2002; Fessler and Westneat, 2007; Lavoué et al., 2013). The absence of

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significant differences in species richness among the Indo-West Pacific, Eastern

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Pacific and Western Atlantic region, provides few clues to inform the origins of the

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Sciaenidae.

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All together it remains unknown when, and by which mechanisms among-region

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diversification occurred. In this study, our objectives were: 1) to reconstruct a

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comprehensive time-calibrated phylogenetic framework of Sciaenidae using a

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multi-gene character set, a rich taxonomic sampling scheme, and several fossils- and

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geology- based time calibration points; and 2) to examine the origin and historical

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biogeography of the sciaenids within this newly built molecular phylogenetic

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framework. We also reconstructed the evolution of the habitat preference through our

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inferred time-tree and determine whether freshwater taxa are the product of a single

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event of freshwater-marine/euryhaline transition or several. We reconstructed the

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ancestral area distributions of the ancestors at nodes using the model of

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“dispersion-extinction-cladogenesis” (Ree and Smith, 2008) to infer the early

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evolutionary history of Sciaenidae.

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2. Materials and methods

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2.1 Taxonomic sampling

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We examined 93 sciaenid taxa within 52 genera sampled from freshwater (8 species within 5 genera) and marine or euryhaline environments. Most of the samples 6

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were collected by the authors. A few specimens and tissues samples were obtained

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through tissue loans and gifts by collaborators (listed in the acknowledgement section)

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and ichthyologic tissue collections, mainly from Scripps Institution of Oceanography,

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USA and Museum and Art Gallery of the Northern Territory, Australia. Specimens

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were identified using morphological traits described in taxonomic references, such as

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“Fishes of Taiwan” (Shen et al., 1993) and the “FAO species identification guide”

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(Séret and Opic, 1990; Sasaki, 2001). Three closely related perciform fishes to

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sciaenids (within the clade N sensu Chen et al. [2007]), Dicentrarchus labrax

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(Moronidae), Monotaxis grandoculis (Lethrinidae) and Sparus aurata (Sparidae),

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were used as out-groups. All species examined in this study are listed in Appendix B

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Table B1, along with the information on their distribution.

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2.2 Character sampling Total genomic DNA was extracted from muscle or fin tissue using a commercial

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DNA extraction kit (DNeasy Blood and Tissue Kit, Qiagen, Hilden) following the

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manufacturer's protocols. The polymerase chain reaction (PCR) was used to amplify

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the following gene fragments: cytochrome b (cyt b), cytochrome oxidase subunit I

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(COI), exon 3 of recombination activating gene 1 (RAG1), intronless rhodopsin (RH),

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exon 2 of early growth response (EGR) 1 gene, and exon 1, intron 1, and exon 2 of

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EGR2B gene. The first two fragments are encoded in the mitochondrial genome and

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the remaining four are part of the nuclear genome. The nuclear loci used are

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phylogenetically informative markers and commonly used for the molecular

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systematics of the ray-finned fishes (Chen et al., 2003; López et al., 2004; Chen et al.,

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2008; Santini et al., 2013a; J-N Chen et al., 2014; W-J Chen et al., 2004a, 2014b).

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Most of the primers used for generating the sequence data from our targeted loci have 7

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been published in previous studies (see supplemental Table B2 in Appendix B for

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their original sources). For this study, we designed a new forward primer (E2B

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ex1PcoF) located at exon 1 of the EGR2B gene that functions with existing reverse

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primers located at the 3’ end of exon 2 to lengthen the amplified fragment from this

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gene. The sequences from EGR2B targeted include the entire intron 1 region of the

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gene, which adds more phylogenetic informative sites suitable for inferring

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intra-familial and intra-generic relationships. It should be noted that the combination

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of the new forward and previously published primers used for EGR2B gene marker

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for sciaenids in this study may also work for other diverse perciform taxa tested in our

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laboratory. Moreover, several cyt b group-specific primers were also designed in this

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study. The sequences of the PCR primers used in this study for each gene marker and

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protocols of PCRs for the makers are provided in Appendix B Table B2.

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PCR products were purified using the AMPure magnetic bead cleanup protocol

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(Agencourt Bioscience Corp). Purified PCR products were sequenced with the same

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primers used in PCRs by Sanger sequencing using dye-labeled terminators and

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dye-labeled fragments read on ABI 3730 analyzers (Applied Biosystems) at Genomics

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BioSci and Tech (Taipei) and the Center of Biotechnology (National Taiwan

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University).

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2.3 Analytical methods

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2.3.1

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Phylogenetic reconstruction

The obtained DNA sequences were edited and aligned with the sequence

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assembly and alignment software, CodonCode Aligner v. 5.0.1 (CodonCode

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Corporation, Dedham, MA, USA) and Se-Al v2.0 (Rambaut, 1996). The possibility of

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sequencing errors resulted from sample mix-up or contamination was checked by

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comparing the topologies of the resulting phylogenetic trees individually inferred

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from each gene fragment and/or comparing to Genbank archived sequences of a

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putatively closely related taxon using BLAST (http://www.ncbi.nlm.nih.gov/BLAST/).

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Manipulation and/or species identification errors were further checked by the

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additional sequence of a second exemplar of the species or of a putatively closely

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related taxon. Finally, the resulting multiple sequence alignments was achieved with

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the automatic multiple alignment program MUSCLE (Edgar, 2004), then adjusted

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manually by eye. Phylogenetic analyses were performed based on the combined DNA sequence

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matrix from the dataset of the six targeted genes mentioned above. A partitioned

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Maximum Likelihood (ML) method (Felsenstein, 1981), as implemented in the

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sequential and parallel program RAxML (version 0.93) (Stamatakis, 2006), was used

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for inferring phylogenies. Partitions were allocated with respect to the six gene

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fragments and to codon positions of each protein-coding gene. Because RAxML only

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provides GTR-related (Yang 1994) models of rate heterogeneity for nucleotide data

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(Stamatakis 2006), the nucleotide substitution model GTR + Γ + I, as implemented in

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RAxML, was employed for the analyses. For each ML search, we conducted five

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independent runs and the final tree with the best ML score was selected among the

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five ML trees of these runs. Nodal support was assessed with bootstrapping

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(Felsenstein, 1985) under the ML criterion, based on 1000 pseudo-replicates

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generated from the five separated runs.

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2.3.2

Divergence time estimation The divergence time estimation (and simultaneous phylogenetic inference) was 9

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based on a Bayesian approach which incorporated a relaxed molecular clock method

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and a set of nine fossil-based calibrations using BEAST v.1.7.5 (Drummond et al.,

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2012). Five independent runs of 5 x 107 generations each were performed. Each run

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was initiated from a user-starting time-tree that we built with BEAST using a GTR

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model of sequence evolution, a strict molecular clock and a single prior age constraint

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for the root of the tree at 65 Ma. Estimation of trees and divergence time were

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sampled once every 5,000 generations and the parameters of each run were checked

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for convergence with the software Tracer v 1.5. We removed the burn-in parts of each

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run (=10%, i.e., 103 trees per run) and the remaining tree samples from the five runs

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were used to reconstruct the maximum clade credibility tree with mean divergence

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times using TreeAnnotator v. 1.5 (Drummond and Rambaut, 2007).

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Our phylogenetic tree was time-calibrated with one sparid and eight sciaenid

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fossils that provide hard minimum age and soft maximum limit ages through an

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exponential distribution in which the 95% credibility interval was equal to the

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maximum age of the strata where the fossil was excavated: 1- The earliest fossil of

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Sparidae, from Paleocene formations of Europe and North Africa, lived 65 Ma (near

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the limit Cretaceous/Paleocene) (Orrell et al., 2002). This fossil is used to constrain

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the time of the most recent common ancestor [tMRCA] of the outgroup clade

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(Monotaxis, Sparus). 2- We use the fossil Umbrina cirrosa (Brzobohatý et al., 2007)

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found in the Kienbergnineyard section (i.e. 14.9-13.7 Ma) to constrain the tMRCA of

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the clade (Umbrina canariensis, U. cirrosa). 3- The oldest fossil of Pachypops

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fourcroi is located in the Pebas Formation (i.e. 23-13.7 Ma) (Monsch, 1998). We use

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this fossil to constrain the tMRCA of the clade (Pachyurus bonariensis, Pachypops

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fourcroi). 4- †Plagioscion marinus is an extinct Plagioscion species from Cantaure

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and Castillo Formation dated to 23-16 Ma (Aguilera and Rodrigues de Aguilera,

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2003). It is used to constrain the tMRCA of the crown group Plagioscion. 5- The 10

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fossil †Genyonemus calvertensis is reported from the early to Middle Miocene

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(17.5-14.5Ma) Plum Point Marl Member of the Calvert Formation (Takeuchi and

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Huddleston, 2008). We use it to constrain the tMRCA of the clade (Genyonemus

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lineatus, Roncador stearnsii). 6- †Equetus davidandrewi from the Early Miocene

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Cantaure Formation (Nolf and Aguilera, 1998) provides us with a minimum age of 16

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Ma and a maximum age of 23 Ma for the clade (Pareques sp., Equetus lanceolatus).

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7- †Larimus henrici and †Larimus steurbauti are two extinct species of Sciaenidae

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from the Early Miocene Cantaure Formation (i.e. 23-16 Ma) (Girone and Nolf, 2009).

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It is used to constrain the tMRCA of the clade (Nebris microps, Larimus pacificus). 8-

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The oldest fossil record of Totoaba is †Totoaba fitchi (Huddleston and Takeuchi, 2007)

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from the late Early Miocene marine upper Olcese Sand (i.e. 17.5-16.7 Ma). This fossil

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is used to constrain the tMRCA of the clade including Totoaba macdonaldi and its

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sister group. 9- We use a fossil specimen of Argyrosomus regius from a Late Langhian

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age for the Kienberg Section (Brzobohatý et al., 2007) to calibrate the minimum age

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of the clade (Argyrosomus regius, A. japonicus) to 13.6 Ma and the maximum age to

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15 Ma.

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2.3.3

Character evolution reconstruction

The ancestral habitat preference was reconstructed on the maximum clade

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credibility tree using the “Mk1” evolutionary model as implemented in Mesquite v.2.

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75 (Maddison and Maddison, 2011). Three character states were recognized for

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habitat preference: marine, euryhaline and freshwater. The habitat preferences of each

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sciaenid examined in this study were collected mainly from FishBase (Froese and

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Pauly, 2011) with additional information from the Catalog of Fish (Eschmeyer, 2013).

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2.3.4

Ancestral area distribution reconstruction

To reconstruct where the ancestors lived, we used the ancestral area reconstruction

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method based on the Dispersal-Extinction-Cladogenesis [DEC] model, as

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implemented in Lagrange version 20130526 (Ree et al., 2005; Ree and Smith, 2008).

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We first defined four biogeographical units based on land constraints, open ocean

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and levels of regional endemicity: Eastern Pacific (EP), Western Atlantic (WA),

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Eastern Atlantic (EA) and Indo-West Pacific (IWP) (Fig. 1B). Each freshwater species

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analyzed in this study were categorized in one of these four oceanic regions based on

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where the rivers in which they live flow into.

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We restricted the maximal ancestral range sizes, that each cannot span more than

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three possible units because most of the species and genera of extant Sciaenidae do

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not live in more than two regions (and usually they are restricted to only one region).

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Furthermore we set up the dispersal rate as 3 between EP and WA before 3.1 Ma

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according to the closure of the Isthmus of Panama and the remaining are 1. Default

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options of other parameters were selected.

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3. Results

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3.1 Phylogenetic Results

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The aligned sequences contain a total of 6619 bp from 93 sciaenid taxa,

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corresponding to the combinations of 1116 bp of cyt b gene, 654 bp of the COI gene,

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1472 bp of the RAG1 gene, 897 bp of the RH gene and 945 bp of the EGR1 gene, as

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well as 1534 bp of the EGR2B gene (including both exon and intron sequence data).

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The partitioned maximum-likelihood and Bayesian analyses support the monophyly 12

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of Sciaenidae (Sasaki, 1989) (Fig. 2-4). The estimated time to the most recent

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common ancestor (MRCA) of Sciaenidae is 27.3 Ma (95% confidence intervals:

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23.1-31.9 Ma) (Fig. 4). Within the inferred phylogenetic tree of the Sciaenidae, we

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identify at least fifteen main groups of Sciaenidae, each with strong statistical support

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(Fig. 2). Nine of these main groups comprise more than one genus. The internal

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branches connecting the main groups are short relative to terminal branches. Eight

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genera for which two species or more species were examined are monophyletic while

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eight others are not (Fig. 2). The eight strictly freshwater sciaenid species (from five

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of six described genera) examined herein form three independent freshwater

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lineages/clades (Fig 2 and 3).

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3.2 Habitat Preference Evolution

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The habitat preference evolution reconstruction indicates that MRCA of the

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Sciaenidae is most likely marine (probability = 0.623) (Fig. 3). Depending on this

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initial habitat preference (marine), there was one event in which an euryhaline

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ancestor became fully marine adapted. This event took place during the Oligocene (i.e.

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transitions 1) (Fig. 3). Then, multiple transitions between marine/euryhaline habitat

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preference occur (at least 21) in six of our main lineages, most of them occur till

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Middle Miocene (Fig. 3). We also observe three independent transitions from

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marine/euryhaline to freshwater habitat preference (transition 2b, lineage 6; transition

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12, Aplodinotus; and transition 16, lineage 11): all of these events may have occurred

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after Oligocene.

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3.3 Ancestral Area Reconstruction

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The ancestral area reconstruction method using the DEC model on our

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time-calibrated tree was used to infer a most likely hypothesis for the distribution of

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MRCA and the region of early diversification of the Sciaenidae (Fig. 4). Our results

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show one highest probability regarding the origin of the crown group Sciaenidae at

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about 27.3 Ma (Late Oligocene): EP (Eastern Pacific) plus WA (Western Atlantic)

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(probability = 0.346). Range expansions, toward EA (Eastern Atlantic) from WA,

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outside the initial region happened twice during the Early Miocene: a first

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trans-Atlantic expansion at about 21.3 Ma (lineage 3) and the second at about 20.6 Ma

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(clade including Aplodinotus, Menticirrhus and lineage 11). Within the lineage 11, a

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vicariant event between EA and IWP gave rise to the diverse endemic IWP

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monophyletic group, at about 16.6 Ma in Early Miocene. A more recent event of

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vicariance between EA and IWP (14 Ma) explains the broad distribution of

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Argyrosomus (Fig. 4).

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4. Discussion

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4.1 Phylogenetic Relationships

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Our molecular study examines by far the most complete taxonomic sampling

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within the Sciaenidae to reconstruct its intra-familiar evolutionary relationships. This

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comprehensive molecular phylogeny allows us to test previous phylogenetic

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hypotheses, to resolve several issues in the systematics of these fishes as well as to

347

reliably reconstruct the historical biogeography of the Sciaenidae. In the inferred

348

phylogenetic tree, we identify fifteen major lineages of Oligocene/Early Miocene age,

349

three of them (lineage 10, Pseudotolithini and Nibeini) (Fig. 2) correspond to three of

350

the subfamilies (Stelliferinae, from subgroup II; Pseudotolithinae and Otolithinae, 14

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from subgroup IV) that Sasaki (1989) proposed (Appendix A). The relationships

352

among most of these main groups remain unresolved. Below we discuss the most

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important results and compare our new findings with the previously proposed

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hypotheses.

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Within lineage 1, Sciaenops and Micropogonias are sister taxa with high bootstrap

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support (Fig. 2). Previous morphology-based studies did not show support for this

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clade (Chao, 1978; Sasaki, 1989). Cynoscion, another important sciaenid genus from

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tropical America, is found within lineage 2 (Fig. 2). This study and previous

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molecular studies (Vinson et al., 2004; Vergara-Chen et al., 2009; Santos et al., 2013)

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reject the hypothesis of the monophyly of Cynoscion based on morphology (Chao,

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1978; Sasaki, 1989).

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Regarding other non-monophyletic genera identified in this study, although we

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sampled only five Umbrina species (out of 18 valid species), we found the genus

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polyphyletic (in lineages 3, 4, and 8) (Fig. 2). Non-monophyly of the genus Sciaena

365

(in lineages 3 and 8) (Fig. 2), which has been suggested by Sasaki based on

366

morphology (1989), is confirmed by the present study. A revised taxonomy for

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Umbrina and Sciaena is necessary, but more work with larger taxonomic sampling is

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needed to fully elucidate the evolution of these problematic genera.

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Lineage 5 contains only one species, Paralonchurus brasiliensis (Fig. 2). Sasaki

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(1989) examined two species of Paralonchurus and suggested this genus was not

371

monophyletic. Currently, no molecular study tests whether this genus is monophyletic

372

or not.

373

Lineage 6 includes exclusively the South American freshwater sciaenids, namely,

374

Pachyurus, Pachypops and Plagioscion (Fig. 2). The present analysis confirms the

375

monophyly of Plagioscion, and its sister-group relationship with the

376

Pachyurus/Pachypops clade (ML bootstrap value = 100%). The same result was 15

16

377

found in Cooke et al. (2012) (based on DNA sequence variation of the mitochondrial

378

ATPase 6/8 and nuclear RAG1 loci; 2292 bp in total). Two other relevant studies, the

379

morphological study of Sasaki (1989) and Santos et al. (2013) based on DNA

380

sequence variation of the mitochondrial 16S, COI and nuclear Tmo-4C4 loci (1362 bp

381

in total with weak statistical support), did not result in the same sister-group

382

relationships for taxa from those genera.

383

Lineage 7 and lineage 8 are diverse lineages, comprising three and seven species

384

respectively, from nine different genera (Fig. 2). Lineage 7 includes Seriphus,

385

Genyonemus and Roncador. Lineage 8 includes Cheilotrema and its sister taxa of the

386

Pareques/Equetus clade, while Cilus/Sciaena deliciosa is sister to the Umbrina

387

roncador/U. xanti. However, none of the taxa mentioned above has been examined

388

simultaneously in previous studies based on either molecular or morphological

389

characters. Here with all the taxa included in the analysis, we confirm the sister-group

390

relationships between Genyonemus and Roncador as well as Pareques and Equetus as

391

Sasaki (1989) suggested. In contrast to the former two lineages, lineage 9 comprises

392

only two genera Nebris and Larimus. Their close relationship is in agreement with the

393

finding from the previous morphological and molecular studies (Santos et al., 2013;

394

Sasaki, 1989).

395

Lineage 10 includes Bairdiella, Corvula, Odontoscion, Ophioscion and Stellifer

396

(Fig. 2). This clade was first suggested by Chao (1978) based on having a

397

two-chambered swim bladder and two enlarged otoliths. Subsequently, Sasaki

398

proposed a subfamily named Stelliferinae for his subgroup II (Appendix A). Within

399

this clade, we find Bairdiella to be the sister taxon of Corvula/Odontoscion with

400

strong support; the genera Ophioscion and Stellifer are not monophyletic; two of the

401

Ophioscion species (O. scierus and O. punctatissimus) are nested within Stellifer

402

whereas the third Ophioscion species (O. vermicularis) is only distantly related to this 16

17

403

group. These relationships are in agreement with Chao’s proposal (Chao, 1978) in

404

which the sister-group relationships between Stellifer and Ophioscion, and between

405

Bairdiella and Odontoscion were suggested. Sasaki (1989) proposed that Corvula was

406

the sister taxon of Odontoscion plus Elattarchus (not sampled in our study).

407

Regarding Corvula, it should be noted that the analysis from the present study shows

408

almost no genetic difference between Corvula macrops and Odontoscion xanthops

409

(Fig. 2). While Corvula does not possess canines as Odontoscion does, the species

410

from this genus are frequently placed in the genus Odontoscion in some taxonomic

411

literature (e.g., Grove and Lavenberg, 1997). This implies that the diagnostic

412

characters such as the presence of canines should further be examined for delimitation

413

of the genera from Corvula, Odontoscion, and Elattarchus. In spite of the uncertainty

414

mentioned above, our combined molecular dataset confirms the non-monophyly of

415

the Stellifer and Ophioscion, as previously noted (Vinson et al. 2004; Santos et al.

416

2013; Barbosa et al. 2014). Santos et al. (2013) who did not examine Corvula and

417

Odontoscion in the Stellifer group in their analysis, found Bairdiella to be the sister

418

taxon of Stellifer/Ophioscion clade (in agreement with our result). Barbosa et al.

419

(2014) examined Stellifer, Ophioscion, Odontoscion and Bairdiella, and found

420

Odontoscion sister to Bairdiella. However, the findings from these molecular studies

421

were based on poorly supported phylogenetic inferences. Finally, despite the fact that

422

sister-group relationships within the Stelliferinae (or lineage 10) have been frequently

423

investigated (e.g., Chao, 1978; Sasaki, 1989; Santos et al., 2013; Barbosa et al., 2014;

424

this study), no conclusive hypothesis was reached. A future molecular study with

425

exhaustive sampling of the Stellifer group concomitant with morphological evidence,

426

is required to reveal stelliferine phylogeny and associated taxonomic implications.

427

The last three lineages in the tree are the North American freshwater Aplodinotus,

428

American king croakers Menticirrhus, and the largest lineage, lineage 11 (Fig. 2). The 17

18

429

present study confirms the monophyly of the genus Menticirrhus (with two species

430

sampled) (Chao, 1978; Vinson et al., 2004; Santos et al., 2013) with strong support.

431

Lineage 11 is the largest lineage (22 genera included) and it can be subdivided

432

into four clades (A-D) although the relationships among these clades are not resolved

433

(Fig. 2). Clade A contains the monotypic Totoaba macdonaldi (indigenous to the Gulf

434

of California in Mexico). Clade B corresponds to the genus Argyrosomus in which the

435

species distributed widely from Eastern Atlantic to Indo-West Pacific.

436

Clade C includes only the West African sciaenids, Pseudotolithus and Pteroscion

437

sampled in this study. This clade is similar to the Pseudotolithini defined by Trewavas

438

(1962) based on their fountain-like unique structure of swim bladder, which was also

439

confirmed by Sasaki (1989). Trewavas (1962) proposed that the tribe Pseudotolithini

440

comprised nine sciaenid species classified within the genera Miracorvina,

441

Pentheroscion, Pteroscion and Pseudotolithus. All these species contain a pair of

442

tube-like appendages divided into several tubules, arising at anterior end of swim

443

bladder (Trewavas, 1962). However, Sasaki (1989) suggested a modified

444

classification of Trewavas (1962) in grouping tribe Pseudotolithini (i.e. Pteroscion

445

and Pseudotolithus) and tribe Miracorviini (i.e. Miracorvina and Pentheroscion) into

446

a subfamily Pseudotolithinae. The present study confirms the monophyly of

447

Pseudotolithini but does not have samples to test the monophyly of Miracorviini. At

448

generic level, our result rejects the monophyly of Pseudotolithus suggested by the

449

previous study (Sasaki, 1989).

450

Clade D consists of diverse endemic Indo-West Pacific sciaenids. Within this

451

clade, three (Larimichthys, Pennahia and Johnius) of the four genera from which we

452

sampled more than one species are monophyletic except for the genus Nibea. The

453

clade D also includes one freshwater species Boesemania microlepis, distributed in

454

Thailand, Vietnam and Sumatra (Froese and Pauly, 2011). 24 out of 31 nodes within 18

19

455

the clade D are well supported (e.g., Boesemania is sister to Panna) with bootstrap

456

values >90% (Fig. 2). However, the resulting relationships are not always consistent

457

with earlier hypotheses. According to Trewavas (1977) (and latter modified by Sasaki

458

[1989]), Nibea, Dendrophysa, Austronibea and Daysciaena belonged to the tribe

459

Nibeini by having the combination of the following morphological characters: five

460

mental pores; a pair of deeply cephalic swim bladder appendages; sagitta with a

461

sharply curved sulcus tail. However, the present study suggests Daysciaena is more

462

closely related to Johnius than other Nibeini members. The taxa from the genus Nibea

463

fall into two different groups: Nibea A (three Nibea species found in Southwest

464

Pacific) and Nibea B (two other Nibea species grouping with Austronibea endemic to

465

Australia, which is sister to Dendrophysa, widely distributed Indo-West Pacific

466

species, but not in Australia). Similar morphological traits can be observed in the two

467

Nibea species in Nibea B, Dendrophysa and Austronibea with the characters of lower

468

jaw teeth uniformly small and an inferior mouth (Sasaki, 1992). These particular

469

features further support our finding for the latter clade and reject the monophyly of

470

Nibea.

471 472 473

4.2 The origin time of the Sciaenidae Xu et al. (2014) examined mitochondrial genome sequence data from 23 sciaenid

474

species and provided a new timescale in which they inferred the age of the Sciaenidae

475

to 208 Ma, a seemingly implausible estimation. It is far older than the oldest

476

acanthomorph fossils that date from the Early Cretaceous, 124-122 Ma (Nolf, 2004)

477

and many others belonging to both stem (e.g., Muhichthys cordobai) and crown

478

lineages of acanthomorphs (polymixiids, beryciformes) which are known from the

479

Late Cretaceous (around 100 Ma) (Patterson 1964; Hatai 1965; Gaudant 1978; Gayet 19

20

480

1980; Otero and Gayet 1996; González-Rodríguez and Fielitz 2008). To calibrate their

481

time-tree, Xu et al. (2014) constrained the age of their ingroup root to 192 Ma, which

482

referred to the split of Tetraodontiformes + Perciformes and other non-perciform.

483

However, this only calibration point (the ingroup root) used was secondarily (and

484

wrongly) inferred from a molecular clock study based on mitogenomic data

485

(Yamanoue et al., 2006) and despite the availability of fossil records from sciaenid

486

and other perciform fishes. The selection of correct calibration points for molecular

487

clock studies is critical for accurate age estimates (Lavoué et al., 2013; W-J Chen et

488

al., 2014b). W.-J. Chen et al. (2014b) pointed out that Yamanoue et al. (2006)

489

incorrectly assigned a 161 Ma old fossil that was originally classified as incertae sedis

490

within Acanthopterygii to Gadiformes, two groups that only date to about 61 Ma in

491

the fossil record (Patterson, 1993).

492

Our study uses nine reliable fossils from related perciform fishes (e.g., Sparidae)

493

as well as relevant sciaenid lineages. We find the crown group Sciaenidae originated

494

at about 27.3 Ma, a dramatically different estimation than Xu et al. (2014). Moreover,

495

our time-tree agrees with recent acanthomorph or percomorph studies based on

496

nuclear loci in inferring a Late Cretaceous/Early Paleogene or younger age for the

497

origin of many of the perciform lineages (Tavera et al., 2012; Near et al., 2013; W-J

498

Chen et al., 2014a, 2014b).

499 500 501

4.3 Evolutionary Habitat Transitions The present study indicates that transitions between marine and euryhaline

502

environments occurred frequently and independently in different lineages in sciaenids

503

and at different periods during the Miocene. This implies that sciaenids can easily

504

adapt to some variations in salinity, possibly as a consequence of inhabiting coastal

20

21

505

habitats and migratory life history (Peters and Jr., 1990; Costa et al., 2014). However,

506

full adaptation to a freshwater environment is a rare event in sciaenids. This result

507

adds to the growing case for suggesting a widespread pattern of biome conservatism

508

among aquatic organisms (i.e., transitions between biomes occurring far less

509

frequently than lineages remaining in their ancestral biome) (Vermeij and Dudley,

510

2000; Wiens and Donoghue, 2004; Wiens and Graham, 2005; Crisp et al., 2009). In

511

fact, we detect only three complete freshwater invasions involving five strictly

512

freshwater sciaenid genera examined (Fig 3 and 4). These three freshwater invasions

513

occurred in three different continents: 1- in South America at 21 Ma (see lineage 6);

514

2- in North America after 19.5 Ma (see Aplodinotus); and 3- in South Asia after 10.3

515

Ma (see Boesemania). The same pattern of independent and sporadic continental

516

freshwater invasions has also been revealed in other fish groups such as

517

Tetraodontidae (Yamanoue et al., 2011), and Engraulidae (Bloom and Lovejoy, 2012).

518

The present study confirms the freshwater colonization of lineage 6 arose in the

519

Early Miocene (Cooke et al., 2012), as a possible by-product of Early Miocene marine

520

incursions (Lovejoy et al., 1998, 2006). Additionally, these results are compatible with

521

a very recent study (Boeger et al. 2014), which suggested that the 23 freshwater

522

sciaenid species in South America sampled in our study evolved from a single

523

freshwater ancestor (Fig. 3). This finding contradicts the previous hypothesis of

524

independent origins for the South American freshwater Sciaenidae (Sasaki, 1989;

525

Santos et al., 2013). Plagioscion may have started to diversify before Pachyurus and

526

Pachypops during Early Miocene to Middle Miocene, a hypothesis congruent with the

527

oldest Plagioscion fossils found in Lower Miocene Cantaure Formation (Aguilera and

528

Rodrigues de Aguilera, 2003). In addition, the sister-group relationship between the

529

South America freshwater sciaenids and Paralonchurus brasiliensis (marine)

530

coincides with the phylogenetic result of their parasites Euryhaliotrema spp. (Boeger 21

22

531

and Kritsky, 2003). These authors also hypothesized that Plagioscion colonized

532

freshwater probably via a marine transgression through western Venezuela that

533

developed before 20 Ma, which is in line with the inference from the present study.

534

The possible causes driving the two other freshwater transitions in North America

535

and Southeast Asia are more difficult to identify because it is not possible to precisely

536

date them: the transition in Aplodinotus may have occurred at any time between the

537

Early Miocene and the present, and the transition of Boesemania may have occurred

538

at any time after the Middle Miocene to the present. Therefore, we can not reject the

539

hypothesis of Barney (1926) who speculated that A. grunniens originated in the Gulf

540

of Mexico before the last glaciations (c.a. 0.012-0.11 Ma).

541 542 543

4.4 Region of Origin and Early Diversification of the Sciaenidae Based on our ancestral area reconstruction (Fig. 4), we suggest the origin of these

544

fishes is EP plus WA. The hypothesis that the ancestor of the sciaenids was distributed

545

worldwide and the region of origin and of early diversification of the Sciaenidae is the

546

IWP region where maximum species richness is observed should herein be rejected.

547

Before the closure of the Isthmus of Panama, EP and WA formed only one

548

“trans-American” maritime region. Thus, the Sciaenidae most likely originated in

549

tropical America or the “New World”. Based on likelihood analysis of ancestral

550

distributions, Xu et al. (2014) reached the same conclusion as they found the center of

551

origin of the Sciaenidae in the “New World”. However, the conclusion of Xu et al.

552

(2014) was internally inconsistent because they also inferred a Jurassic/Triassic age of

553

the Sciaenidae. At that time, the “Old” and “New” Worlds were not yet separated as

554

both formed part of the Pangaea supercontinent.

555

A tropical New World origin of the Sciaenidae is also congruent with the fossil 22

23

556

record. The earliest fossil record of sciaenids is a worn otolith from the Bashi Marl,

557

Lower Eocene of Mississippi (Nolf, 1995). The Sciaenidae were absent during

558

Eocene along the Pacific coast of North America while there are abundant otolith

559

fossils from other fish groups at that period. The otolith fossils became more abundant

560

in the Oligocene and Neogene terrigenous beds of Europe and America (Bannikov et

561

al., 2009; Fierstine et al., 2012; Bannikov, 2013). Yet sciaenid fossils appeared

562

frequently in Asia only from the younger Cenozoic deposits (Hatai, 1965). This

563

pattern suggests that the earliest occurrence of Sciaenidae is indeed in tropical

564

America (New World), especially the Atlantic region (Nolf, 2003). Afterward, this

565

family might have invaded the Eastern Pacific from the Gulf Coast region through the

566

Panamanian Seaway after the Eocene (Huddleston and Takeuchi, 2006), and finally

567

reached other regions.

568 569 570

4.5 Origin of Current Distribution and Diversity Pattern of the Sciaenidae The present-day distribution of the Sciaenidae in EA and IWP resulted from two

571

early range expansions outside the New World after the Oligocene based on the

572

results of our analyses. One of the expansions led to the formation of the EA clade in

573

lineage 3 (Fig. 4). This result indicates the Sciaena and Umbrina species inhabiting

574

the EA region share a most recent common ancestor, making these two widespread

575

distributed genera non-monophyletic.

576

The other expansion contributed to the highly diverse linage 11 (Fig. 4) whose

577

most recent common ancestor was distributed in EP plus IWP at 18.2 Ma. Subsequent

578

speciation event split it into two groups; one comprises those species living currently

579

in EP (Totoaba macdonaldi) and IWP plus EA (wide-distributed genus Argyrosomus);

580

other includes the EA (or endemic West African) sciaenid genera and the remaining 23

24

581

18 endemic IWP genera. The terminal Tethyan event (TTE) approximately

582

mid-Burdigalian (c. 19.2 – 17.2 Ma) to Langhian (c. 15.97 – 13.65 Ma) (Adams et al.,

583

1983; Steininger and Rögl, 1979) is often hypothesized to cause the cut off of

584

low-latitude gene flow of marine animals from the IWP and the EA (Adams et al.,

585

1983) due to the consequence of large-scale changes in the global ocean circulation

586

(Von Der Heydt and Dijkstra, 2006; Groeneveld et al., 2007). The two vicariant events

587

identified within lineage 11 (Fig. 4) might be related directly or indirectly to the TTE,

588

one of these vicariant events gave rise to the initial diversification of the

589

widely-distributed genus Argyrosomus (14 Ma). Conversely, in some cases (i.e.,

590

labroid and pomacentrid genera as well as marine gastropods), the initial speciation

591

occurred prior to the TTE as suggested from both molecular dating studies and fossil

592

records (Rosen and Smith, 1988; Malaquias and Reid, 2009; Cowman and Bellwood,

593

2013).

594

The vicariance of western African sciaenids (EA clade) from the IWP clade at

595

12.8 Ma may have been assisted by features of ocean circulation seen today.

596

Numerous studies have investigated the global ocean circulation and its significance

597

in shaping species distributions in marine vertebrates and invertebrates (Chow et al.,

598

2000; Tolley et al., 2005; Groeneveld et al., 2007; Henriques et al., 2014).

599

Accordingly, Henriques et al. (2014) suggested that the Benguela current system first

600

formed at 12-10 Mya (Diester-Haass et al., 1990; Krammer et al., 2006) in South

601

Africa may have driven one population of a sciaenid species (Atractoscion aequidens)

602

to be isolated from another. A similar mechanism could have occurred here in our

603

case.

604

Finally, the crown group of around 90 IWP species diversified starting at 16.6 Ma.

605

Our results support a mechanism of within area diversifications in new environmental

606

niches probably driven by adaptive radiation (Liem, 1990; Schluter, 2000) from a 24

25

607

single IWP sciaenid ancestor during the Miocene. This would explain the current

608

pattern of species richness in the IWP that hosts 33.6% of sciaenid species. Certainly,

609

an advanced study should be carried out to better understand the causes of such a

610

pattern of rapid species diversification in relation to ecology and morphology (e.g.,

611

complex feature in swim bladder found especially in IWP sciaenids).

612

613

614

5. Conclusion

Recent systematic treatments of marine teleosts have mostly focused on

615

scleractinian coral reef-associated perciform lineages (Price et al., 2011; Frédérich et

616

al., 2013; Santini et al., 2013a, 2013b). Fewer studies included other lineages that

617

represent also a vast proportion of marine fish biodiversity. Sciaenidae, a large and

618

world-wide distributed perciform family comprising approximately 300 species, is

619

one of such little investigated lineages in which many questions on systematics,

620

taxonomy, and biogeography remain unanswered. This study represents the most

621

comprehensive investigation of the family to date. Our molecular dating shows the

622

crown group originated about 27.3 Ma in the tropical America where its early

623

diversification occurred. Later eastward dispersal events, subsequent diversification

624

via vicariates (EA vs. IWP), and within region (e.g., IWP) diversification are

625

hypothesized to account for their current global distribution and species diversity

626

patterns. Finally, the South-American freshwater sciaenids form a monophyletic

627

group that is not related to the North-American nor Asian freshwater sciaenids. This

628

result suggests three independent transitions in three different continents from

629

marine/euryhaline to freshwater environments.

630

25

26

631

Acknowledgements

632

The authors wish to thank Sébastien Lavoué and Matthew Campbell for their helpful

633

discussions and comments in relevance to this manuscript. We thank Gavin Dally,

634

Jean-Dominique Durant, Kent Carpenter, Millicent Sanciangco, Ramon Ruiz-Carus,

635

Richard L. Mayden, Samuel Iglésia, Scripps Institution of Oceanography (via H.-J.

636

Walker), and Museum and Art Gallery of the Northern Territory, Australia (via

637

Michael Hammer) for the loan or gift of tissue samples. This work was supported by

638

research grants from the Ministry of Science and Technology, Taiwan (MOST

639

101-2611-M-002 -016 -MY3 to WJC).

640

26

27

641

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Figure legends Figure 1. Geographical pattern of distribution of the Sciaenidae. (A) Distribution and species diversity of Sciaenidae. Number of species per grid cell (4 by 4 degree latitude-longitude resolution) is represented by cool (low diversity) to warm (high diversity) colors. Individual species distribution compiled from FishBase (Froese and Pauly, 2011). (B) The four biogeographical units used in the ancestral ranges reconstruction analysis. For each region, total number of sciaenid species is indicated respectively in parentheses.

966 Figure 2. Phylogenetic tree of Sciaenidae constructed with the partitioned maximum likelihood method based on the combined dataset using GTR + Γ + I model. Branch lengths are proportional to inferred nucleotide substitutions. Numbers at nodes represent bootstrap values in percentage. Values below 70％ are not shown. Asterisk indicates the genera do not appear to be monophyletic in the tree; the tree is rooted with sparoid perciformes (Monotaxis grandoculis and Sparus aurata). 967 Figure 3. Reconstruction of the evolution of salinity preference within the Sciaenidae using likelihood optimization on the Bayesian time-calibrated tree. The phylogenetic chronogram is inferred with BEAST v. 1.7.5 (Drummond et al., 2012), using the combined dataset, calibrated with nine fossil-based constraints (see text for details). Outgroups are deleted for the analysis. Horizontal timescale shows in millions of years ago. Salinity preference classified in three states: “marine or mainly marine” show in white, “euryhaline” in gray, and “strictly freshwater” in black. The relative probabilities of each state are drawn using pie charts at each node. Numbered black arrowheads show habitat transitions. The Gray background-color indicates the

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39

duration of Early Miocene. Vertical black arrow indicates the closure of Isthmus of Panama. 968 Figure 4. Most likely ancestral ranges reconstruction of the Sciaenidae using the dispersal-extinction-cladogenesis (DEC) model (Ree et al., 2005; Ree and Smith, 2008) onto a simplified Bayesian phylogenetic chronogram. Outgroups are deleted for the analysis. Horizontal timescale shows in millions of years ago. Most likely ancestral ranges reconstruction at nodes indicates by code-color boxes. Areas depicted are: Eastern Pacific (orange), Western Atlantic (green), Eastern Atlantic (blue), and Indo-West Pacific (yellow) (see Figure 1B for correspondence). The blue background-color indicates the duration of Early Miocene. Vertical black arrow shows the closure of Isthmus of Panama. Salinity preference transition events show with while arrowheads. Nodes without code-color box indicate within region diversification. Branches in red represent the dispersal events predating or likely predating Early Miocene, and branches in green indicate the transition from marine/euryhaline to freshwater. The black stars show subsequent allopatric cladogenesis. 969 970 971

Appendix A

972 973

Table A1 List of four main sciaenid subgroups into ten subfamilies Sasaki’s described

with their distribution.

974 975

Appendix B Supplemental materials

39

40

976 977

Table B1 Taxa, gene and GenBank accession numbers gene sequences of

978

Table B2 Primers and PCR protocols used in this study.

representative species.

979 980 981

40

1-5 6-10 11-15 16-20 21-25 26-30 31-35 36-40

A

EA

(17/19)

IWP

EP (82/82) WA Eastern Pacific (EP) Western Atlantic (WA) Eastern Atlantic (EA) Indo-West Pacific (IWP)

B

Fig 1 (Lo et al.)

(82/82)

(91/93)

100

100

Fig 2 (Lo et al.)

Monotaxis grandoculis Sparus aurata Dicentrarchus labrax Sciaenops ocellatus 94 100 Micropogonias furnieri Micropogonias undulatus Micropogonias ectenes 79 Cynoscion guatucupa Atractoscion nobilis Cynoscion reticulatus 100 100 Cynoscion regalis Cynoscion acoupa 100 100 Cynoscion parvipinnis Macrodon ancylodon 79 Isopisthus remifer 100 100 Cynoscion praedatorius 100 Sciaena umbra Umbrina canariensis 93 Umbrina cirrosa Leiostomus xanthurus Pogonias cromis Umbrina bussingi 100 Paralonchurus brasiliensis Pachyurus bonariensis 100 Pachypops fourcroi Plagioscion auratus 100 100 Plagioscion surinaensis Plagioscion ternetzi 99 89 Plagioscion squamosissimus Seriphus politus 95 Genyonemus lineatus Roncador stearnsii 70 Cheilotrema saturnum 100 Pareques sp. 100 Equetus lanceolatus 99 Cilus gilberti 100 Sciaena deliciosa Umbrina roncador 100 94 Umbrina xanti 97 Nebris microps Larimus pacificus Bairdiella cf. armata 99 Bairdiella ronchus 100 100 Corvula macrops 2 Corvula macrops 1 100 Odontoscion xanthops Ophioscion vermicularis Stellifer microps Stellifer ericymba Stellifer oscitans 100 71 Stellifer rastrifer 94 100 Ophioscion scierus Ophioscion punctatissimus Aplodinotus grunniens Menticirrhus americanus 100 Menticirrhus undulatus A Totoaba macdonaldi B Argyrosomus regius Argyrosomus japonicus 100 83 Pseudotolithus elongatus C 100 Pteroscion peli Pseudotolithus brachygnathus 72 85 100 Pseudotolithus senegalensis Pseudotolithus typus Miichthys miiuy 99 Bahaba taipingensis Collichthys lucidus 100 Larimichthys polyactis 93 Larimichthys crocea D Boesemania microlepis 100 100 Panna microdon 91 Atrobucca nibe Otolithes ruber 100 89 Pterotolithus maculatus Chrysochir aureus 100 Protonibea diacanthus 98 99 Megalonibea fusca 100 Pennahia macrocephalus Pennahia pawak 100 100 Pennahia argentata Nibea albiflora 100 Nibea chui 100 Nibea soldado Dendrophysa russelii 100 Nibea squamosa 98 Nibea microgenys 95 100 Austronibea oedogenys Daysciaena albida Johnius amblycephalus 97 Johnius macropterus 100 Johnius majan Johnius distinctus 100 Johnius borneensis 99 Johnius carouna 100 Johnius belangerii Johnius heterolepis 95 88 Johnius trewavasae

0.1

Outgroup Sciaenops

Lineage 1

Micropogonias Cynoscion* Cynoscion*

Lineage 2

Cynoscion* Sciaena* Umbrina* Leiostomus Pogonias Umbrina*

Lineage 3 Lineage 4 Lineage 5 Lineage 6

Plagioscion Seriphus Genyonemus Roncador Cheilotrema

Lineage 7

Lineage 8

Cilus Sciaena* Umbrina*

Lineage 9 Bairdiella Corvula* Ophioscion*

Stelliferinae

Lineage 10

Stellifer* Ophioscion* Aplodintus Menticirrhus Totoaba Argrosomus Pseudotolithus* Pteroscion Pseudotolithus*

Pseudotolithini

Miichthys Larimichthys Boesemania

Chrysochir Protonibea Megalonibea

Lineage 11

Pennahia Nibea* A Dendrophysa Nibea* B Austronibea Daysciaena

Johnius

Nibeini

30

20

10

0 (Mya)

2a

2b

1

3 4

5 6 7

8

9

10 11 12 13

14 15

17

16

18

19 20

21

22 23 24

25

Paleogene Oligocene

Neogene Miocene

Q Pliocene

Leiostomus xanthurus Umbrina bussingi Paralonchurus brasiliensis Pachyurus bonariensis Pachypops fourcroi Plagioscion auratus Plagioscion surinaensis Plagioscion squamosissimus Plagioscion ternetzi Seriphus politus Genyonemus lineatus Roncador stearnsii Cheilotrema saturnum Equetus lanceolatus Pareques sp. Umbrina xanti Umbrina roncador Cilus gilberti Sciaena deliciosa Larimus pacificus Nebris microps Bairdiella cf. armata Bairdiella ronchus Corvula macrops Odontoscion xanthops Corvula macrops Ophioscion vermicularis Stellifer microps Stellifer ericymba Stellifer rastrifer Stellifer oscitans Ophioscion scierus Ophioscion punctatissimus Pogonias cromis Sciaena umbra Umbrina cirrosa Umbrina canariensis Sciaenops ocellatus Micropogonias undulatus Micropogonias ectenes Micropogonias furnieri Cynoscion guatucupa Atractoscion nobilis Cynoscion regalis Cynoscion reticulatus Cynoscion acoupa Cynoscion parvipinnis Macrodon ancylodon Cynoscion praedatorius Isopisthus remifer Aplodinotus grunniens Menticirrhus undulatus Menticirrhus americanus Totoaba macdonaldi Argyrosomus regius Argyrosomus japonicus Pseudotolithus elongatus Pteroscion peli Pseudotolithus brachygnathus Pseudotolithus typus Pseudotolithus senegalensis Miichthys miiuy Bahaba taipingensis Collichthys lucidus Larimichthys polyactis Larimichthys crocea Panna microdon Boesemania microlepis Atrobucca nibe Otolithes ruber Pterotolithus maculatus Chrysochir aureus Protonibea diacanthus Megalonibea fusca Pennahia macrocephalus Pennahia argentata Pennahia pawak Nibea albiflora Nibea soldado Nibea chui Dendrophysa russelii Nibea squamosa Nibea microgenys Austronibea oedogenys Daysciaena albida Johnius amblycephalus Johnius macropterus Johnius majan Johnius borneensis Johnius distinctus Johnius carouna Johnius belangerii Johnius trewavasae Johnius heterolepis

Leiostomus Lineage 4 Lineage 5 Lineage 6

Lineage 7

Lineage 8

Lineage 9

Lineage 10

Pogonias Lineage 3 Lineage 1

Lineage 2

Aplodinotus Menticirrhus

Lineage 11

Fig 4 (Lo et al.)

30

20 24.1

10 2a 15

21

23.5

16.7

2b

25.3

19

1 22.4

27.3

0 (Mya)

17.5

18.2

16.5

21 17.5

23.9

17.8 3

22.1

7.4 10.2

4

15.7 26.4

5

13.4

6

12.4

11.2

7

4 8.9 3.2

21.3

16 8

15.8

5.4

19.2

23.4

11.5 9

15.9

8

12.6

6.3 11.2

10

8.7

11

5.7

22.2 12

19.5

20.6

2.3

13

7.5 17.1

14 12.8

18.2

17.6

14 15 10.3

16.6 17

16

16 15.4 18

19 20

21

22 23 24

25

Paleogene Oligocene

Neogene Miocene

Leiostomus xanthurus Umbrina bussingi Paralonchurus brasiliensis Pachyurus bonariensis Pachypops fourcroi Plagioscion auratus Plagioscion surinaensis Plagioscion squamosissimus Plagioscion ternetzi Seriphus politus Genyonemus lineatus Roncador stearnsii Cheilotrema saturnum Equetus lanceolatus Pareques sp. Umbrina xanti Umbrina roncador Cilus gilberti Sciaena deliciosa Larimus pacificus Nebris microps Bairdiella cf. armata Bairdiella ronchus Corvula macrops Odontoscion xanthops Corvula macrops Ophioscion vermicularis Stellifer microps Stellifer ericymba Stellifer rastrifer Stellifer oscitans Ophioscion scierus Ophioscion punctatissimus Pogonias cromis Sciaena umbra Umbrina cirrosa Umbrina canariensis Sciaenops ocellatus Micropogonias undulatus Micropogonias ectenes Micropogonias furnieri Cynoscion guatucupa Atractoscion nobilis Cynoscion regalis Cynoscion reticulatus Cynoscion acoupa Cynoscion parvipinnis Macrodon ancylodon Cynoscion praedatorius Isopisthus remifer Aplodinotus grunniens Menticirrhus undulatus Menticirrhus americanus Totoaba macdonaldi Argyrosomus regius Argyrosomus japonicus Pseudotolithus elongatus Pteroscion peli Pseudotolithus brachygnathus Pseudotolithus typus Pseudotolithus senegalensis Miichthys miiuy Bahaba taipingensis Collichthys lucidus Larimichthys polyactis Larimichthys crocea Panna microdon Boesemania microlepis Atrobucca nibe Otolithes ruber Pterotolithus maculatus Chrysochir aureus Protonibea diacanthus Megalonibea fusca Pennahia macrocephalus Pennahia argentata Pennahia pawak Nibea albiflora Nibea soldado Nibea chui Dendrophysa russelii Nibea squamosa Nibea microgenys Austronibea oedogenys Daysciaena albida Johnius amblycephalus Johnius macropterus Johnius majan Johnius borneensis Johnius distinctus Johnius carouna Johnius belangerii Johnius trewavasae Johnius heterolepis

Leiostomus Lineage 4 Lineage 5 Lineage 6

Lineage 7

Lineage 8

Lineage 9

Lineage 10

Pogonias Lineage 3 Lineage 1

Lineage 2

Aplodinotus Menticirrhus

Lineage 11

Q Pliocene

Fig 4 (Lo et al.)

41

982 983

•

The historical biogeography of the global Sciaenidae is reconstructed.

984

•

The family originated and diversified in the tropical America during Early Miocene.

985 986

•

Fifteen major lineages of Oligocene/Early Miocene age are identified.

987

•

The center of origin hypothesis cannot explain sciaenid species richness in IWP.

988

•

Three independent transitions from marine to freshwater environments occurred.

989

41

(82 spp.) 11.9 Ma 26.1 Ma

(19 spp.)

(82 spp.) 16.7 Ma

(93 spp.)