A multi-gene dataset reveals a tropical New World origin and EarlyMiocene diversification of croakers (Perciformes: Sciaenidae) q

Pei-Chun Lo a, Shu-Hui Liu a, Ning Labbish Chao b, Francis K.E. Nunoo c, Hin-Kiu Mok d, Wei-Jen Chen a,⇑a Institute of Oceanography, National Taiwan University, No. 1, Sec. 4 Roosevelt Road, Taipei 10617, Taiwanb National Museum of Marine Biology & Aquarium, No. 2, Houwan Road, Checheng, Pingtung 94450, Taiwanc Department of Marine and Fisheries Sciences, University of Ghana, Legon, Accra, Ghanad Department of Oceanography, National Sun Yat-Sen University, No. 70, Lienhai Road, Kaohsiung 80424, Taiwan

a r t i c l e i n f o

Article history:Received 5 February 2015Revised 26 March 2015Accepted 28 March 2015Available online 4 April 2015

Keywords:BiogeographyIndo-West PacificNew WorldSciaenidaeSystematicsTime-calibrated phylogeny

a b s t r a c t

Widely distributed groups of living animals, such as the predominantly marine fish family Sciaenidae,have always attracted the attention of biogeographers to document the origins and patterns of diversifi-cation in time and space. In this study, the historical biogeography of the global Sciaenidae is recon-structed within a molecular phylogenetic framework to investigate their origin and to test thehypotheses explaining the present-day biogeographic patterns. Our data matrix comprises six mitochon-drial and nuclear genes in 93 globally sampled sciaenid species from 52 genera. Within the inferredphylogenetic tree of the Sciaenidae, we identify 15 main and well-supported lineages; some of whichhave not been recognized previously. Reconstruction of habitat preferences shows repeated habitat tran-sitions between marine and euryhaline environments. This implies that sciaenids can easily adapt tosome variations in salinity, possibly as the consequence of their nearshore habitats and migratory life his-tory. Conversely, complete marine/euryhaline to freshwater transitions occurred only three times, inSouth America, North America and South Asia. Ancestral range reconstruction analysis concomitant withfossil evidence indicates that sciaenids first originated and diversified in the tropical America during theOligocene to Early Miocene before undergoing two range expansions, to Eastern Atlantic and to the Indo-West Pacific where a maximum species richness is observed. The uncommon biogeographic pattern iden-tified is discussed in relation to current knowledge on origin of gradients of marine biodiversity towardthe center of origin hypothesis in the Indo-West Pacific.

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1. Introduction

Sciaenids are commonly called croakers or drums because oftheir propensity to produce sounds using sonic muscles and swimbladder (Tower, 1908; Ramcharitar et al., 2006). These soundsmight be species- or sex-specific and are used for communication(Mok and Gilmore, 1983; Myrberg, 1997; Amorim and Hawkins,2000; Ladich, 2004; Gannon, 2007; Kasumyan, 2009; Mok et al.,2009). This particular feature makes sciaenids attractive modelsfor acoustic-related research focusing on the behaviors, matechoice, and evolution (Connaughton et al., 2000; Gannon, 2007;Aalbers, 2008). In spite of their attractive acoustic behavior, thetaxonomy, biogeography, and evolutionary relationships among

the species remain largely uncertain, primarily due to absence ofa comprehensive phylogeny for sciaenids.

Sciaenids form one of the largest families of the Perciformes,comprising 66 genera and approximately 291 species (Eschmeyerand Fong, 2013). Anatomical examination supports its monophylybut does not identify its sister group (Sasaki, 1989). Currentadvances on molecular phylogenetics of the Percomorpha do notresolve the sister group of Sciaenidae but circumscribe a restrictivelist of possibilities within the clade N sensu Chen et al. (2007). Thisclade includes also some of the major groups of tropical fishesinhabiting coral reefs (e.g., Chaetodontidae, Lethrinidae,Tetraodontiformes) and blackish water (e.g., Haemulidae), as wellas major temperate water lineages (e.g., Moronidae, Sparidae),and deep-sea taxa (e.g., Lophiiformes) (Chen et al., 2007;Betancur-R et al., 2013; Near et al., 2013; W.-J. Chen et al., 2014b).

Chao (1978) first assessed the phylogenetic relationships of allwestern Atlantic sciaenids and placed them into 11 generic groupsbased on their swim bladder, otoliths and external morphology.The most comprehensive revision for the systematics of the

http://dx.doi.org/10.1016/j.ympev.2015.03.0251055-7903/! 2015 Elsevier Inc. All rights reserved.

q This paper has been recommended for acceptance by Giacomo Bernardi⇑ Corresponding author at: Room 301, Institute of Oceanography, National

Taiwan University, No. 1, Sec. 4 Roosevelt Road, Taipei 10617, Taiwan. Fax: +8862 23637062.

E-mail address: wjchen.actinops@gmail.com (W.-J. Chen).

Molecular Phylogenetics and Evolution 88 (2015) 132–143

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Sciaenidae was made by Sasaki (1989) who proposed a newphylogenetic hypothesis based on a cladistic analysis of severalosteological and myological characters and a large taxonomic sam-pling with 87 species (from 60 genera) distributed worldwide.Accordingly, Sasaki (1989) revised the classification of Sciaenidaeby dividing the family into four synapomorphy-based subgroups:I, II, III and IV (Supplementary data 1 in Appendix A), yet therelationships among the subgroups and within the subgroupsremain mostly unresolved.

All previous molecular phylogenetic studies of the Sciaenidaewere limited to few taxa, a particular geographical region, and onlymitochondrial markers were used to infer the relationships(Vinson et al., 2004; Vergara-Chen et al., 2009; Cooke et al.,2012; Santos et al., 2013; Barbosa et al., 2014). Due to their limitedtaxonomic samplings, none of these molecular studies provided ageneral test of Sasaki’s (1989) hypothesis and others that allow abetter understanding of evolution of the global Sciaenidae, forinstance, the historical hypotheses explaining their currentdistribution patterns.

Sciaenids are distributed worldwide in coastal zones of tropicaland temperate regions (Chao, 1978, 1986; Sasaki, 1989). Most ofthe species are marine. A few species (euryhaline) are able to adaptto a wide range of salinities. However, only about 25 species in sixgenera strictly inhabit freshwaters in North America (one species),South America (23 species) and Southeast Asia (one species)(Casatti, 2002). The distribution of Sciaenidae and their speciesdiversity pattern across the oceanic regions are summarized inFig. 1. Widely distributed groups of living animals, such as thefamily Sciaenidae, have always attracted the attention of bio-geographers to document the origins and patterns of diversifica-tion in time and space. In fact, the historical factors andprocesses leading to the present-day biogeographic patterns havealready been studied in some of the important fish groups suchas Clupeoidei (sardines and anchovies) (Lavoué et al., 2013),Otophysi (including major freshwater water lineages of the teleostfishes) (Chen et al., 2013), Percichthyoidea (temperate freshwaterperch-like fishes) (W.-J. Chen et al., 2014a), and Tetraodontidae(pufferfishes) (Yamanoue et al., 2011; Santini et al., 2013), yet

Fig. 1. Geographical pattern of distribution of the Sciaenidae. (A) Distribution and species diversity. Number of species per grid cell (4 by 4 degree latitude–longituderesolution) is represented by cool (low diversity) to warm (high diversity) colors. Individual species distribution compiled from FishBase (Froese and Pauly, 2011). (B) The fourbiogeographical units used in the ancestral range reconstruction analysis. For each region, number of endemic and total number of species are indicated respectively inparentheses.

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there are no conclusive hypothesis proposed for the highly diverseSciaenidae.

Sasaki (1989) was the first to concretely discuss the historicalbiogeography and evolutionary origin of the Sciaenidae using hisphylogenetic results. Three alternative hypotheses were consid-ered: 1 – the ancestor of Sciaenidae was distributed worldwidewith subsequent diversification predominantly occurring viavicariant events; 2 – New World origin of the ancestor with east-ward and/or westward dispersal (favored hypothesis of Sasaki); 3– Old World origin of the ancestor with eastward and/or westwarddispersal. Because of a general lack of phylogenetic resolutionamong the main groups of sciaenids, it was difficult to objectivelychoose the best biogeographical hypothesis for this group. Despitethe fact that fossil records might be indicative for studying the his-torical biogeography, Sasaki (1989) did not consider fossil data inhis analysis.

Regarding the species diversity pattern, the sciaenid speciesrichness among regions is somewhat atypical as it is not stronglyunbalanced (Fig. 1) as it can be observed in several other groupsof fishes and other marine animals. Typically, the Indo-WestPacific region comprises more species than any other regions inmost of the worldwide-distributed marine groups (Tittensoret al., 2010). In sciaenids, the respective numbers of species inthe Indo-West Pacific, Eastern Pacific and Western Atlantic regionsare comparable with about 82–93 species per region. It is some-times assumed that the region of maximal diversity is also theregion of origin of a group of organisms (Briggs, 1999, 2003;Orrell et al., 2002; Santini and Winterbottom, 2002; Fessler andWestneat, 2007; Lavoué et al., 2013). The absence of significant dif-ferences in species richness among the Indo-West Pacific, EasternPacific and Western Atlantic region, provides few clues to informthe origins of the Sciaenidae.

All together it remains unknown when, and by which mecha-nisms among-region diversification occurred. In this study, ourobjectives were: (1) to reconstruct a comprehensive time-cali-brated phylogenetic framework of the Sciaenidae using a multi-gene character set, a rich taxonomic sampling scheme, and severalfossils-based time calibration points; and (2) to examine the originand historical biogeography of sciaenids within this newly builtmolecular phylogenetic framework. We also reconstructed theevolution of the habitat preference through our inferred time-treeand determine whether freshwater taxa are the product of a singleevent of freshwater–marine/euryhaline transition or several. Wereconstructed the ancestral area distributions of the ancestors atnodes using the model of ‘‘Dispersion–Extinction–Cladogenesis’’(Ree and Smith, 2008) to infer the early evolutionary history ofthe Sciaenidae.

2. Materials and methods

2.1. Taxonomic sampling

We examined 93 sciaenid taxa within 52 genera sampled fromfreshwater (8 species within 5 genera) and marine or euryhalineenvironments. Most of the samples were collected by the authors.A few samples were obtained through tissue loans and gifts by col-laborators (listed in the acknowledgment section) and ichthyologictissue collections, mainly from Scripps Institution ofOceanography, USA and Museum and Art Gallery of the NorthernTerritory, Australia. Specimens were identified using morphologi-cal traits described in taxonomic references, such as ‘‘Fishes ofTaiwan’’ (Shen et al., 1993) and the ‘‘FAO species identificationguide’’ (Séret and Opic, 1990; Sasaki, 2001). Three closely relatedperciform fishes to sciaenids (within the clade N sensu Chen et al.[2007]), Dicentrarchus labrax (Moronidae), Monotaxis grandoculis

(Lethrinidae) and Sparus aurata (Sparidae), were used as out-groups. All species examined in this study are listed in Table S2of supplementary data 2 in Appendix A, along with the informationon their distribution.

2.2. Character sampling

Total genomic DNA was extracted from muscle or fin tissueusing a commercial DNA extraction kit (DNeasy Blood and TissueKit, Qiagen, Hilden) following the manufacturer’s protocols. Thepolymerase chain reaction (PCR) was used to amplify the followinggene fragments: cytochrome b (cyt b), cytochrome oxidase subunitI (COI), exon 3 of recombination activating gene 1 (RAG1), intron-less rhodopsin (RH), exon 2 of early growth response (EGR) 1 gene,and exon 1, intron 1, and exon 2 of EGR2B gene. The first two frag-ments are encoded in the mitochondrial genome and the remain-ing four are part of the nuclear genome. The nuclear loci used arephylogenetically informative markers and commonly used for themolecular systematics of the ray-finned fishes (Chen et al., 2003;López et al., 2004; Chen et al., 2008; Santini et al., 2013; J.-N.Chen et al., 2014; W.-J. Chen et al., 2014a,b). Most of the primersused for generating the sequence data from our targeted loci havebeen published in previous studies (see Table S3 of supplementarydata 2 in Appendix A for their original sources). For this study, wedesigned a new forward primer (E2B ex1PcoF) located at exon 1 ofthe EGR2B gene that functions with existing reverse primerslocated at the 30 end of exon 2 to lengthen the amplified fragmentfrom this gene. The sequences from targeted EGR2B include theentire intron 1 region of the gene, which adds more phylogeneticinformative sites suitable for inferring intra-familial and intra-gen-eric relationships. It should be noted that the combination of thenew forward and previously published primers used for EGR2Bgene marker for sciaenids in this study may also work for otherdiverse perciform taxa tested in our laboratory. Moreover, severalcyt b group-specific primers were also designed in this study.The sequences of the PCR primers for each gene marker and proto-cols of PCRs used in this study are provided in Table S3 of supple-mentary data 2 in Appendix A.

The obtained PCR products were purified using the AMPuremagnetic bead cleanup protocol (Agencourt Bioscience Corp).Purified PCR products were sequenced with the same primers usedin PCRs by Sanger sequencing using dye-labeled terminators anddye-labeled fragments read on ABI 3730 analyzers (AppliedBiosystems) at Genomics BioSci and Tech (Taipei) and the Centerof Biotechnology (National Taiwan University).

2.3. Analytical methods

2.3.1. Phylogenetic reconstructionThe obtained DNA sequences were edited and aligned with the

sequence assembly and alignment software, CodonCode Aligner v.5.0.1 (CodonCode Corporation, Dedham, MA, USA) and Se–Al v2.0(Rambaut, 1996). The possibility of sequencing errors resultedfrom sample mix-up or contamination was checked by comparingthe topologies of the resulting phylogenetic trees individuallyinferred from each gene fragment and/or comparing to Genbankarchived sequences of a putatively closely related taxon usingBLAST (http://www.ncbi.nlm.nih.gov/BLAST/). Manipulation and/or species identification errors were further checked by the addi-tional sequence of a second exemplar of the species or of a puta-tively closely related taxon. Finally, the resulting multiplesequence alignments was achieved with the automatic multiplealignment program MUSCLE (Edgar, 2004), then adjusted manuallyby eye.

Phylogenetic analyses were performed based on the combinedDNA sequence matrix from the dataset of the six targeted genes

134 P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143

mentioned above. A partitioned Maximum Likelihood (ML) method(Felsenstein, 1981), as implemented in the sequential and parallelprogram RAxML (version 0.93) (Stamatakis, 2006), was used forinferring phylogenies. Partitions were allocated with respect tothe six gene fragments and to codon positions of each protein-cod-ing gene. Because RAxML only provides GTR-related (Yang, 1994)models of rate heterogeneity for nucleotide data (Stamatakis,2006), the nucleotide substitution model GTR + C + I, as imple-mented in RAxML, was employed for the analyses. For each MLsearch, we conducted five independent runs and the final tree withthe best ML score was selected among the five ML trees ofthese runs. Nodal support was assessed with bootstrapping(Felsenstein, 1985) under the ML criterion, based on 1000pseudo-replicates generated from the five separated runs.

2.3.2. Divergence time estimationThe divergence time estimation (and simultaneous phyloge-

netic inference) was based on a Bayesian approach which incorpo-rated a relaxed molecular clock method and a set of nine fossil-based calibrations using BEAST v.1.7.5 (Drummond et al., 2012).Five independent runs of 5 ! 107 generations each were per-formed. Each run was initiated from a user-starting time-tree thatwe built with BEAST using a GTR model of sequence evolution, astrict molecular clock and a single prior age constraint for the rootof the tree at 65 Ma. Estimation of trees and divergence time weresampled once every 5000 generations and the parameters of eachrun were checked for convergence with the software Tracer v1.5. We removed the burn-in parts of each run (=10%, i.e., 103

trees per run) and the remaining tree samples from the five runswere used to reconstruct the maximum clade credibility tree withmean divergence times using TreeAnnotator v. 1.5 (Drummondand Rambaut, 2007).

Our phylogenetic tree was time-calibrated with one sparid andeight sciaenid fossils that provide hard minimum age and softmaximum limit ages through an exponential distribution in whichthe 95% credibility interval was equal to the maximum age of thestrata where the fossil was excavated: 1 – The earliest fossil ofSparidae, from Paleocene formations of Europe and North Africa,lived 65 Ma (near the limit Cretaceous/Paleocene) (Orrell et al.,2002). This fossil is used to constrain the time of the most recentcommon ancestor [tMRCA] of the outgroup clade (Monotaxis,Sparus). 2 – We use the fossil Umbrina cirrosa (Brzobohaty et al.,2007) found in the Kienbergnineyard section (i.e., 14.9–13.7 Ma)to constrain the tMRCA of the clade (Umbrina canariensis, U. cir-rosa). 3 – The oldest fossil of Pachypops fourcroi is located in thePebas Formation (i.e., 23–13.7 Ma) (Monsch, 1998). We use thisfossil to constrain the tMRCA of the clade (Pachyurus bonariensis,Pachypops fourcroi). 4 – !Plagioscion marinus is an extinctPlagioscion species from Cantaure and Castillo Formation dated to23–16 Ma (Aguilera and Rodrigues de Aguilera, 2003). It is usedto constrain the tMRCA of the crown group Plagioscion. 5 – The fos-sil !Genyonemus calvertensis is reported from the early to MiddleMiocene (17.5–14.5 Ma) Plum Point Marl Member of the CalvertFormation (Takeuchi and Huddleston, 2008). We use it to constrainthe tMRCA of the clade (Genyonemus lineatus, Roncador stearnsii). 6– !Equetus davidandrewi from the Early Miocene CantaureFormation (Nolf and Aguilera, 1998) provides us with a minimumage of 16 Ma and a maximum age of 23 Ma for the clade (Parequessp., Equetus lanceolatus). 7 – !Larimus henrici and !Larimus steur-bauti are two extinct species of Sciaenidae from the EarlyMiocene Cantaure Formation (i.e., 23–16 Ma) (Nolf and Aguilera,1998). It is used to constrain the tMRCA of the clade (Nebrismicrops, Larimus pacificus). 8 – The oldest fossil record of Totoabais !Totoaba fitchi (Huddleston and Takeuchi, 2007) from the lateEarly Miocene marine upper Olcese Sand (i.e., 17.5–16.7 Ma).This fossil is used to constrain the tMRCA of the clade including

Totoaba macdonaldi and its sister group. 9 – We use a fossil speci-men of Argyrosomus regius from a Late Langhian age for theKienberg Section (Brzobohaty et al., 2007) to calibrate the mini-mum age of the clade (Argyrosomus regius, A. japonicus) to13.6 Ma and the maximum age to 15 Ma.

2.3.3. Character evolution reconstructionThe ancestral habitat preference was reconstructed on the

maximum clade credibility tree using the ‘‘Mk1’’ evolutionarymodel as implemented in Mesquite v.2.75 (Maddison andMaddison, 2011). Three character states were recognized for habi-tat preference: marine, euryhaline and freshwater. The habitat pre-ferences of each sciaenid examined in this study were collectedmainly from FishBase (Froese and Pauly, 2011) with additionalinformation from the Catalog of Fish (Eschmeyer, 2013).

2.3.4. Ancestral area reconstructionTo reconstruct where the ancestors lived, we used the ancestral

area reconstruction method based on the Dispersal–Extinction–Cladogenesis [DEC] model, as implemented in Lagrange version20130526 (Ree et al., 2005; Ree and Smith, 2008).

We first defined four biogeographical units based on land con-straints, open ocean and levels of regional endemicity: EasternPacific (EP), Western Atlantic (WA), Eastern Atlantic (EA) andIndo-West Pacific (IWP) (Fig. 1B). Each freshwater species analyzedin this study were categorized in one of these four oceanic regionsbased on where the rivers in which they live flow into.

We restricted the maximal ancestral range sizes, that each can-not span more than three possible units because most of the spe-cies and genera of extant Sciaenidae do not live in more thantwo regions (and usually they are restricted to only one region).Furthermore we set up the dispersal rate as 3 between EP andWA before 3.1 Ma according to the closure of the Isthmus ofPanama and the remaining are 1. Default options of other parame-ters were selected.

3. Results

3.1. Phylogenetic results

The aligned sequences contain a total of 6619 bp from 93 sci-aenid taxa, corresponding to the combinations of 1116 bp of cytb gene, 654 bp of the COI gene, 1473 bp of the RAG1 gene, 897 bpof the RH gene and 945 bp of the EGR1 gene, as well as 1534 bpof the EGR2B gene (including both exon and intron sequence data).The partitioned maximum-likelihood and Bayesian analyses sup-port the monophyly of Sciaenidae (Sasaki, 1989) (Figs. 2–4). Theestimated time to the most recent common ancestor (MRCA) ofSciaenidae is 27.3 Ma (95% confidence intervals: 23.1–31.9 Ma)(Fig. 4). Within the inferred phylogenetic tree of the Sciaenidae,we identify at least fifteen main groups of Sciaenidae, each withstrong statistical support (Fig. 2). Nine of these main groups com-prise more than one genus. The internal branches connecting themain groups are short relative to terminal branches. Eight generafor which two or more species were examined are monophyleticwhile eight others are not (Fig. 2). The eight strictly freshwater sci-aenid species (from five of six described genera) examined hereinform three independent freshwater lineages/clades (Figs. 2 and 3).

3.2. Habitat preference evolution

The habitat preference evolution reconstruction indicates thatMRCA of the Sciaenidae is most likely euryhaline (probabil-ity = 0.623) (Fig. 3). Depending on this initial habitat preference(euryhaline), there was one event in which an euryhaline ancestor

P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143 135

became fully marine adapted. This event took place during theOligocene (i.e., transitions 1) (Fig. 3). Then, multiple transitionsbetween marine/euryhaline habitat preference occur (at least 22)

in seven of our main lineages, most of them occur till MiddleMiocene (Fig. 3). We also observe three independent transitionsfrom marine/euryhaline to freshwater habitat preference

Fig. 2. Phylogenetic tree of the Sciaenidae constructed with the partitioned maximum likelihood method based on the combined dataset using GTR + C + I model. Branchlengths are proportional to inferred nucleotide substitutions. Numbers at nodes represent bootstrap values in percentage. Values below 70% are not shown. Asterisk indicatesthe genera do not appear to be monophyletic in the tree; the tree is rooted with sparoid perciformes (Monotaxis grandoculis and Sparus aurata).

136 P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143

Fig. 3. Reconstruction of the evolution of salinity preference within the Sciaenidae using likelihood optimization onto the Bayesian time-calibrated tree. The phylogeneticchronogram is inferred with BEAST v. 1.7.5 (Drummond et al., 2012) based on 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’’ 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 showhabitat transitions. The gray vertical indicates the duration of the Early Miocene. Vertical black arrow indicates the closure of Isthmus of Panama.

P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143 137

Fig. 4. Most likely ancestral range reconstruction of the Sciaenidae using the Dispersal–Extinction–Cladogenesis (DEC) model (Ree et al., 2005; Ree and Smith, 2008) onto thesimplified Bayesian phylogenetic chronogram constructed in this study. Outgroups are deleted for the analysis. Horizontal timescale shows in millions of years ago. Mostlikely ancestral range reconstruction at nodes indicates by code-color boxes. Areas depicted are: Eastern Pacific (orange), Western Atlantic (green), Eastern Atlantic (blue), andIndo-West Pacific (yellow) (see Fig. 1B for correspondence). The light blue vertical indicates the duration of the Early Miocene. Vertical black arrow shows the closure ofIsthmus of Panama. White arrowheads show salinity preference transition events. Nodes without code-color box indicate within region diversifications. Branches in redrepresent the dispersal events predating or likely predating Early Miocene, and branches in green indicate the transition from marine/euryhaline to freshwater. The blackstars show subsequent allopatric cladogenesis.

138 P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143

(transition 2b, lineage 6; transition 12, Aplodinotus; and transition16, lineage 11): all of these events may have occurred afterOligocene.

3.3. Ancestral area reconstruction

The ancestral area reconstruction method using the DEC modelon our time-calibrated tree was used to infer a most likelyhypothesis for the distribution of MRCA and the region of earlydiversification of the Sciaenidae (Fig. 4). Our results show onehighest probability regarding the origin of the crown groupSciaenidae at about 27.3 Ma (Late Oligocene): EP (Eastern Pacific)plus WA (Western Atlantic) (probability = 0.346). Range expan-sions, toward EA (Eastern Atlantic) from WA, outside the initialregion happened twice during the Early Miocene: a first trans-Atlantic expansion at about 21.3 Ma (clade including lineage 3and Pogonias) and the second at about 20.6 Ma (clade includingAplodinotus, Menticirrhus and lineage 11). Within the lineage 11,a vicariant event between EA and IWP gave rise to the diverseendemic IWP monophyletic group, at about 17.6 Ma in EarlyMiocene. A more recent event of vicariance between EA and IWP(14 Ma) explains the broad distribution of Argyrosomus (Fig. 4).

4. Discussion

4.1. Phylogenetic relationships

Our molecular study examines by far the most complete taxo-nomic sampling within the Sciaenidae to reconstruct its intra-familiar evolutionary relationships. This comprehensive molecularphylogeny allows us to test previous phylogenetic hypotheses, toresolve several issues in the systematics of these fishes as well asto reliably reconstruct the historical biogeography of theSciaenidae. In the inferred phylogenetic tree, we identify fifteenmajor lineages of Oligocene/Early Miocene age, three of them (lin-eage 10, Pseudotolithini and Nibeini) (Figs. 2–4) correspond tothree of the subfamilies (Stelliferinae, from subgroup II;Pseudotolithinae and Otolithinae, from subgroup IV) that Sasaki(1989) proposed (see supplementary data 1 in Appendix A). Therelationships among most of these main groups remain unre-solved. Below we discuss the most important results and compareour new findings with the previously proposed hypotheses.

Within lineage 1, Sciaenops and Micropogonias are sister taxawith high bootstrap support (Fig. 2). Previous morphology-basedstudies did not show support for this clade (Chao, 1978; Sasaki,1989). Cynoscion, another important sciaenid genus from tropicalAmerica, is found within lineage 2 (Fig. 2). This study and pre-vious molecular studies (Vinson et al., 2004; Vergara-Chenet al., 2009; Santos et al., 2013) reject the hypothesis of themonophyly of Cynoscion based on morphology (Chao, 1978;Sasaki, 1989).

Regarding other non-monophyletic genera identified in thisstudy, although we sampled only five Umbrina species (out of 18valid species), we found the genus polyphyletic (in lineages 3, 4,and 8) (Fig. 2). Non-monophyly of the genus Sciaena (in lineages3 and 8) (Fig. 2), which has been suggested by Sasaki based on mor-phology (1989), is confirmed by the present study. A revised taxon-omy for Umbrina and Sciaena is necessary, but more work withlarger taxonomic sampling is needed to fully elucidate the evolu-tion of these problematic genera.

Lineage 5 contains only one species, Paralonchurus brasiliensis(Fig. 2). Sasaki (1989) examined two species of Paralonchurus andsuggested this genus was not monophyletic. Currently, no molecu-lar study tests whether this genus is monophyletic or not.

Lineage 6 includes exclusively the South American freshwatersciaenids, namely, Pachyurus, Pachypops and Plagioscion (Fig. 2).The present analysis confirms the monophyly of Plagioscion, andits sister-group relationship with the Pachyurus/Pachypops clade(ML bootstrap value = 100%). The same result was found in Cookeet al. (2012) (based on DNA sequence variation of the mitochon-drial ATPase 6/8 and nuclear RAG1 loci; 2292 bp in total). Two otherrelevant studies, the morphological study of Sasaki (1989) andSantos et al. (2013) based on DNA sequence variation of themitochondrial 16S, COI and nuclear Tmo-4C4 loci (1362 bp in totalwith weak statistical support), did not result in the same sister-group relationships for taxa from those genera.

Lineage 7 and lineage 8 are diverse lineages, comprising threeand seven species respectively, from nine different genera(Fig. 2). Lineage 7 includes Seriphus, Genyonemus and Roncador.Lineage 8 includes Cheilotrema and its sister taxa of the Pareques/Equetus clade, while Cilus gilberti/Sciaena deliciosa is sister to theUmbrina roncador/U. xanti. However, none of the taxa mentionedabove has been examined simultaneously in previous studiesbased on either molecular or morphological characters. Here withall the taxa included in the analysis, we confirm the sister-grouprelationships between Genyonemus and Roncador as well asPareques and Equetus as Sasaki (1989) suggested. In contrast tothe former two lineages, lineage 9 comprises only two generaNebris and Larimus. Their close relationship is in agreement withthe finding from the previous morphological and molecular studies(Santos et al., 2013; Sasaki, 1989).

Lineage 10 includes Bairdiella, Corvula, Odontoscion, Ophioscionand Stellifer (Fig. 2). This clade was first suggested by Chao(1978) based on having a two-chambered swim bladder and twoenlarged otoliths. Subsequently, Sasaki (1989) proposed a subfam-ily named Stelliferinae for his subgroup II (see supplementary data1 in Appendix A). Within this clade, we find Bairdiella to be the sis-ter taxon of Corvula/Odontoscion with strong support; the generaOphioscion and Stellifer are not monophyletic; two of theOphioscion species (O. scierus and O. punctatissimus) are nestedwithin Stellifer whereas the third Ophioscion species (O. vermicu-laris) is only distantly related to this group. These relationshipsare in agreement with Chao’s proposal (Chao, 1978) in which thesister-group relationships between Stellifer and Ophioscion, andbetween Bairdiella and Odontoscion were suggested. Sasaki (1989)proposed that Corvula was the sister taxon of Odontoscion plusElattarchus (not sampled in our study). Regarding Corvula, it shouldbe noted that the analysis from the present study shows almost nogenetic difference between Corvula macrops and Odontoscion xan-thops (Fig. 2). While Corvula does not possess canines asOdontoscion does, the species from this genus were frequentlyplaced in the genus Odontoscion in some taxonomic literature(e.g., Grove and Lavenberg, 1997). This implies that the diagnosticcharacters such as the presence of canines should further be exam-ined for delimitation of the genera from Corvula, Odontoscion, andElattarchus. In spite of the uncertainty mentioned above, our com-bined molecular dataset confirms the non-monophyly of theStellifer and Ophioscion, as previously noted (Vinson et al., 2004;Santos et al., 2013; Barbosa et al., 2014). Santos et al. (2013) whodid not examine Corvula and Odontoscion in the Stellifer group intheir analysis, found Bairdiella to be the sister taxon of Stellifer/Ophioscion clade (in agreement with our result). Barbosa et al.(2014) examined Stellifer, Ophioscion, Odontoscion and Bairdiella,and found Odontoscion sister to Bairdiella. However, the findingsfrom these molecular studies were based on poorly supportedphylogenetic inferences. Finally, despite the fact that sister-grouprelationships within the Stelliferinae (or lineage 10) have been fre-quently investigated (e.g., Chao, 1978; Sasaki, 1989; Santos et al.,2013; Barbosa et al., 2014; this study), no conclusive hypothesiswas reached. A future molecular study with exhaustive sampling

P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143 139

of the Stellifer group concomitant with morphological evidence, isrequired to reveal stelliferine phylogeny and associated taxonomicimplications.

The last three lineages in the tree are the North American fresh-water Aplodinotus, American king croakers Menticirrhus, and thelargest lineage, lineage 11 (Fig. 2). The present study confirmsthe monophyly of the genus Menticirrhus (with two species sam-pled) (Chao, 1978; Vinson et al., 2004; Santos et al., 2013) withstrong support.

Lineage 11 is the largest lineage (22 genera included) and it canbe subdivided into four clades (A–D) although the relationshipsamong these clades are not resolved (Fig. 2). Clade A contains themonotypic Totoaba macdonaldi (indigenous to the Gulf ofCalifornia in Mexico). Clade B corresponds to the genusArgyrosomus in which the species distributed widely fromEastern Atlantic to Indo-West Pacific.

Clade C includes only the West African sciaenids, Pseudotolithusand Pteroscion sampled in this study. This clade is similar to thePseudotolithini defined by Trewavas (1962) based on their foun-tain-like unique structure of swim bladder, which was also con-firmed by Sasaki (1989). Trewavas (1962) proposed that the tribePseudotolithini comprised nine sciaenid species classifiedwithin the genera Miracorvina, Pentheroscion, Pteroscion andPseudotolithus. All these species contain a pair of tube-like appen-dages divided into several tubules, arising at anterior end of swimbladder (Trewavas, 1962). However, Sasaki (1989) suggested amodified classification of Trewavas (1962) in grouping tribePseudotolithini (i.e., Pteroscion and Pseudotolithus) and tribeMiracorviini (i.e., Miracorvina and Pentheroscion) into a subfamilyPseudotolithinae. The present study confirms the monophyly ofPseudotolithini but does not have samples to test the monophylyof Miracorviini. At generic level, our result rejects the monophylyof Pseudotolithus suggested by the previous study (Sasaki, 1989).

Clade D consists of diverse endemic Indo-West Pacific sciaenids.Within this clade, three (Larimichthys, Pennahia and Johnius) of thefour genera from which we sampled more than one species aremonophyletic except for the genus Nibea. The clade D also includesone freshwater species Boesemania microlepis, distributed inThailand, Vietnam and Sumatra (Froese and Pauly, 2011). 24 outof 31 nodes within the clade D are well supported (e.g.,Boesemania is sister to Panna) with bootstrap values >90%(Fig. 2). However, the resulting relationships are not always consis-tent with earlier hypotheses. According to Trewavas (1977) (andlatter modified by Sasaki [1989]), Nibea, Dendrophysa, Austronibeaand Daysciaena belonged to the tribe Nibeini by having the com-bination of the following morphological characters: five mentalpores; a pair of deeply cephalic swim bladder appendages; sagittawith a sharply curved sulcus tail. However, the present study sug-gests Daysciaena is more closely related to Johnius than otherNibeini members. The taxa from the genus Nibea fall into two dif-ferent groups: Nibea A (three Nibea species found in SouthwestPacific) and Nibea B (two other Nibea species grouping withAustronibea endemic to Australia, which is sister to Dendrophysacontaining widely distributed Indo-West Pacific species, but notrestrictedly in Australia). Similar morphological traits can beobserved in the two Nibea species in Nibea B, Dendrophysa andAustronibea with the characters of lower jaw teeth uniformly smalland an inferior mouth (Sasaki, 1992). These particular featuresfurther support our finding for the latter clade and reject themonophyly of Nibea.

4.2. The origin time of the Sciaenidae

Xu et al. (2014) examined mitochondrial genome sequence datafrom 23 sciaenid species and provided a new timescale in whichthey inferred the age of the Sciaenidae to 208 Ma, a seemingly

implausible estimation. It is far older than the oldest acantho-morph fossils that date from the Early Cretaceous, 124–122 Ma(Nolf, 2004) and many others belonging to both stem (e.g.,Muhichthys cordobai) and crown lineages of acanthomorphs (poly-mixiids, beryciformes) which are known from the Late Cretaceous(around 100 Ma) (Patterson, 1964; Hatai, 1965; Gaudant, 1978;Gayet, 1980; Otero and Gayet, 1996; González-Rodríguez andFielitz, 2008). To calibrate their time-tree, Xu et al. (2014) con-strained the age of their ingroup root to 192 Ma, which referredto the split of Tetraodontiformes + Perciformes and other non-per-ciform. However, this only calibration point (the ingroup root)used was secondarily (and wrongly) inferred from a molecularclock study based on mitogenomic data (Yamanoue et al., 2006)and despite the availability of fossil records from sciaenid andother perciform fishes. The selection of correct calibration pointsfor molecular clock studies is critical for accurate age estimates(W.-J. Chen et al., 2014b). W.-J. Chen et al. (2014b) pointed out thatYamanoue et al. (2006) incorrectly assigned a 161 Ma old fossilthat was originally classified as incertae sedis withinAcanthopterygii to Gadiformes, two groups that only date to about61 Ma in the fossil record (Patterson, 1993).

Our study uses nine reliable fossils from related perciformfishes (e.g., Sparidae) as well as relevant sciaenid lineages. We findthe crown group Sciaenidae originated at about 27.3 Ma, a dra-matically different estimation than Xu et al. (2014). Moreover,our time-tree agrees with recent acanthomorph or percomorphstudies based on nuclear loci in inferring a Late Cretaceous/EarlyPaleogene or younger age for the origin of many of the perciformlineages (Tavera et al., 2012; Near et al., 2013; W.-J. Chen et al.,2014a,b; Santini et al., 2014; Santini and Carnevale, 2015).

4.3. Evolutionary habitat transitions

The present study indicates that transitions between marineand euryhaline environments occurred frequently and indepen-dently in different lineages in sciaenids and at different periodsduring the Miocene. This implies that sciaenids can easily adaptto some variations in salinity, possibly as a consequence of inhabit-ing coastal habitats and migratory life history (Peters andMcMichael, 1990; Costa et al., 2014). However, full adaptation toa freshwater environment is a rare event in sciaenids. This resultadds to the growing case for suggesting a widespread pattern ofbiome conservatism among aquatic organisms (i.e., transitionsbetween biomes occurring far less frequently than lineagesremaining in their ancestral biome) (Vermeij and Dudley, 2000;Wiens and Donoghue, 2004; Wiens and Graham, 2005; Crispet al., 2009). In fact, we detect only three complete freshwaterinvasions involving five strictly freshwater sciaenid genera exam-ined (Figs. 3 and 4). These three freshwater invasions occurred inthree different continents: 1 – in South America at 21 Ma (see lin-eage 6); 2 – in North America after 19.5 Ma (see Aplodinotus); and 3– in South Asia after 10.3 Ma (see Boesemania). The same pattern ofindependent and sporadic continental freshwater invasions hasalso been revealed in other fish groups such as Tetraodontidae(Yamanoue et al., 2011), and Engraulidae (Bloom and Lovejoy,2012).

The present study confirms the freshwater colonization of lin-eage 6 arose in the Early Miocene (Cooke et al., 2012), as a possibleby-product of Early Miocene marine incursions (Lovejoy et al.,1998, 2006). Additionally, these results are compatible with a veryrecent study (Boeger et al., 2015), which suggested that the 23freshwater sciaenid species in South America sampled in our studyevolved from a single freshwater ancestor (Fig. 3). This finding con-tradicts the previous hypothesis of independent origins for theSouth American freshwater Sciaenidae (Sasaki, 1989; Santoset al., 2013). Plagioscion may have started to diversify before

140 P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143

Pachyurus and Pachypops during Early Miocene to Middle Miocene,a hypothesis congruent with the oldest Plagioscion fossils found inLower Miocene Cantaure Formation (Aguilera and Rodrigues deAguilera, 2003). In addition, the sister-group relationship betweenthe South America freshwater sciaenids and Paralonchurusbrasiliensis (marine) coincides with the phylogenetic result of theirparasites Euryhaliotrema spp. (Boeger and Kritsky, 2003). Theseauthors also hypothesized that Plagioscion colonized freshwaterprobably via a marine transgression through western Venezuelathat developed before 20 Ma, which is in line with the inferencefrom the present study.

The possible causes driving the two other freshwater transitionsin North America and Southeast Asia are more difficult to identifybecause it is not possible to precisely date them: the transition inAplodinotus may have occurred at any time between the EarlyMiocene and the present, and the transition of Boesemania mayhave occurred at any time after the Middle Miocene to the present.Therefore, we cannot reject the hypothesis of Barney (1926) whospeculated that A. grunniens originated in the Gulf of Mexico beforethe last glaciations (c. 0.012–0.11 Ma).

4.4. Region of origin and early diversification of the Sciaenidae

Based on our ancestral area reconstruction (Fig. 4), we suggestthe origin of these fishes is EP plus WA. The hypothesis that theancestor of the sciaenids was distributed worldwide and the regionof origin and of early diversification of the Sciaenidae is the IWPregion where maximum species richness is observed should hereinbe rejected.

Before the closure of the Isthmus of Panama, EP and WA formedonly one ‘‘trans-American’’ maritime region. Thus, the Sciaenidaemost likely originated in tropical America or the ‘‘New World’’.Based on likelihood analysis of ancestral distributions, Xu et al.(2014) reached the same conclusion as they found the center oforigin of the Sciaenidae in the ‘‘New World’’. However, the conclu-sion of Xu et al. (2014) was internally inconsistent because theyalso inferred a Jurassic/Triassic age of the Sciaenidae. At that time,the ‘‘Old’’ and ‘‘New’’ Worlds were not yet separated as bothformed part of the Pangaea supercontinent.

A tropical New World origin of the Sciaenidae is also congruentwith the fossil record. The earliest fossil record of sciaenids is aworn otolith from the Bashi Marl, Lower Eocene of Mississippi(Nolf, 1995). The Sciaenidae were absent during Eocene along thePacific coast of North America while there are abundant otolith fos-sils from other fish groups at that period. The otolith fossils becamemore abundant in the Oligocene and Neogene terrigenous beds ofEurope and America (Bannikov et al., 2009; Fierstine et al., 2012;Bannikov, 2013). Yet sciaenid fossils appeared frequently in Asiaonly from the younger Cenozoic deposits (Hatai, 1965). This pat-tern suggests that the earliest occurrence of Sciaenidae is indeedin tropical America (New World), especially the Atlantic region(Nolf, 2003). Afterward, this family might have invadedthe Eastern Pacific from the Gulf Coast region through thePanamanian Seaway after the Eocene (Huddleston and Takeuchi,2006), and finally reached other regions.

4.5. Origin of current distribution and diversity pattern of theSciaenidae

The present-day distribution of the Sciaenidae in EA and IWPresulted from two early range expansions outside the New Worldafter the Oligocene based on the results of our analyses. One ofthe expansions led to the formation of the EA clade in lineage 3(Fig. 4). This result indicates the Sciaena and Umbrina species inha-biting the EA region share a most recent common ancestor, makingthese two widespread distributed genera non-monophyletic.

The other expansion contributed to the highly diverse linage 11(Fig. 4) whose most recent common ancestor was distributed in EPplus IWP at 18.2 Ma. Subsequent speciation event split it into twogroups; one comprises those species living currently in EP (Totoabamacdonaldi) and IWP plus EA (wide-distributed genusArgyrosomus); other includes the EA (or endemic West African)sciaenid genera and the remaining 18 endemic IWP genera. Theterminal Tethyan event (TTE) approximately mid-Burdigalian (c.19.2–17.2 Ma) to Langhian (c. 16.0–13.7 Ma) (Adams et al., 1983;Steininger and Rögl, 1979) is often hypothesized to cause the cutoff of low-latitude gene flow of marine animals from the IWPand the EA (Adams et al., 1983) due to the consequence of large-scale changes in the global ocean circulation (Von der Heydt andDijkstra, 2006; Groeneveld et al., 2007). The two main vicariantevents identified within lineage 11 (Fig. 4) might be relateddirectly or indirectly to the TTE, one of these vicariant events gaverise to the initial diversification of the widely-distributed genusArgyrosomus (14 Ma). Conversely, in some cases (i.e., labroid andpomacentrid genera as well as marine gastropods), the initialspeciation occurred prior to the TTE as suggested from bothmolecular dating studies and fossil records (Rosen and Smith,1988; Malaquias and Reid, 2009; Cowman and Bellwood, 2013).

The vicariance of western African sciaenids (EA clade) from theIWP clade at 17.6 Ma may have been assisted by features of oceancirculation seen today. Numerous studies have investigated theglobal ocean circulation and its significance in shaping species dis-tributions in marine vertebrates and invertebrates (Chow et al.,2000; Tolley et al., 2005; Groeneveld et al., 2007; Henriqueset al., 2014). Accordingly, Henriques et al. (2014) suggested thatthe Benguela current system first formed at 12–10 Ma (Diester-Haass et al., 1990; Krammer et al., 2006) in South Africa may havedriven one population of a sciaenid species (Atractoscion aequidens)to be isolated from another. A similar mechanism could haveoccurred here in our case.

Finally, the crown group of around 90 IWP species diversifiedstarting at 16.6 Ma. Our results support a mechanism of withinarea diversifications in new environmental niches probably drivenby adaptive radiation (Liem, 1990; Schluter, 2000) from a singleIWP sciaenid ancestor during the Miocene. This would explainthe current pattern of species richness in the IWP that hosts33.6% of sciaenid species. Certainly, an advanced study should becarried out to better understand the causes of such a pattern ofrapid species diversification in relation to ecology and morphology(e.g., complex feature in swim bladder found especially in IWPsciaenids).

5. Conclusion

Recent systematic treatments of marine teleosts have mostlyfocused on scleractinian coral reef-associated perciform lineages.Fewer studies included other lineages that represent also a vastproportion of marine fish biodiversity. Sciaenidae, a large andworld-wide distributed perciform family comprising approxi-mately 300 species, is one of such little investigated lineages inwhich many questions on systematics, taxonomy, and bio-geography remain unanswered. This study represents the mostcomprehensive investigation of the family to date. Our moleculardating shows the crown group originated about 27.3 Ma in thetropical America where its early diversification occurred. Latereastward dispersal events, subsequent diversification via vicariates(EA vs. IWP), and within region (e.g., IWP) diversification arehypothesized to account for their current global distribution andspecies diversity patterns. Finally, the South-American freshwatersciaenids form a monophyletic group that is not related to theNorth-American nor Asian freshwater sciaenids. This result

P.-C. Lo et al. / Molecular Phylogenetics and Evolution 88 (2015) 132–143 141

suggests three independent transitions in three different conti-nents from marine/euryhaline to freshwater environments.

Acknowledgments

The authors wish to thank Sébastien Lavoué and MatthewCampbell for their helpful discussions and comments on the rele-vance to this manuscript. We thank Gavin Dally, Jean-DominiqueDurant, Kent Carpenter, Millicent Sanciangco, Ramon Ruiz-Carus,Richard L. Mayden, Samuel Iglésia, Scripps Institution ofOceanography (via H.-J. Walker), and Museum and Art Gallery ofthe Northern Territory, Australia (via Michael Hammer) for theloan or gift of tissue samples. This work was supported by researchgrants from the Ministry of Science and Technology, Taiwan (MOST101-2611-M-002-016-MY3 to WJC). NLC thanks the support fromGlobal Sciaenidae Conservation Network organized by NMMBA,Taiwan.

Appendix A. Supplementary material

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.ympev.2015.03.025.

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