Diversity, phylogeny, and historical biogeography of large-eye seabreams (Teleostei: Lethrinidae)

Highlights

• Diversity and phylogeny in the Monotaxinae (large-eye seabreams) is investigated.

• Monophyly of all four genera in the Monotaxinae is confirmed.

• 15 species within Gymnocranius are reported, four of which are new.

• The historical biogeography of the Monotaxinae is reconstructed.

• The Monotaxinae originated and diversified in the central Indo-West Pacific.

• The center-of-origin hypothesis is supported to explain the species diversity pattern.

Abstract

The large-eye seabreams or Monotaxinae is one of two subfamilies in the Lethrinidae, a family of perch-like coral reef fishes. Despite its widespread occurrence and its commercial interest in the tropical Indo-West Pacific (IWP), this subfamily has traditionally been considered a taxonomically difficult group. Based on 268 samples collected from all 15 known large-eye seabream species throughout their distribution ranges, we investigated the taxonomic diversity and phylogenetic relationships in the subfamily. From the results of multiple analyses on four gene markers, we confirmed the monophyly of all four genera in the subfamily (Gnathodentex, Gymnocranius, Monotaxis and Wattsia). We confirmed the occurrence of two species in the genus Monotaxis. We reported 15 delimited species within the most speciose genus Gymnocranius, four of which are potentially new species. The time-calibrated phylogenetic reconstruction enabled us to clarify the evolutionary history of the large-eye seabreams and to infer past patterns of species distribution. The most recent common ancestor to the Monotaxinae likely occurred in the central IWP ca. 32 million years ago. A burst of species diversification likely took place during the Mid- to Late Miocene, coinciding with tectonic change in the central IWP region. This gave rise to most extant lineages in Gymnocranius. The observed geographic distribution patterns in the subfamily most likely point to the central IWP as the area of origin and diversification. This was followed by multiple events of centrifugal range expansion towards either the Indian Ocean or the western Pacific Ocean, or both. Our results thus provide new support for S. Ekman’s center-of-origin hypothesis.

Introduction

The Indo-West Pacific (IWP) is the Earth’s largest marine biogeographical region (Crandall and Riginos, 2014). The marine species richness of the IWP reaches its maximum in the Coral Triangle, a geographic region that extends from south of Taiwan in the North, to Bali in the South-West and to the Solomon islands in the East (Hoeksema, 2007). Over 3000 reef fish species have been recorded in the Coral Triangle whereas the total species richness is only a few hundreds in the outer regions of the IWP. Although this peculiar spatial pattern of species richness has been well recognized, we are only beginning to decipher its origin in relation with past geological, climate and evolutionary events (Hoeksema, 2007, Barber, 2009, Halas and Winterbottom, 2009, Carpenter et al., 2011, Briggs and Bowen, 2013, Cowman and Bellwood, 2013, Lavoué et al., 2013, Sanciangco et al., 2013, Lo et al., 2015). The volume of empirical data necessary to test hypotheses that explain the diversity gradient centered in the Coral Triangle and to understand the underlying evolutionary mechanisms is still limited. Comparative phylogeographic and phylogenetic surveys of species from various marine zoological groups are still needed to investigate the major evolutionary patterns and processes at play (Rocha and Bowen, 2008).

In this study, a group of medium- to large-sized coral reef fishes occurring exclusively in the IWP from the subfamily Monotaxinae of the Lethrinidae was investigated. This subfamily, commonly known as large-eye seabreams currently comprises 15 described, and one undescribed species. The species are classified in four genera of which Gymnocranius is the most speciose, with so far 11 described, and one undescribed species (Carpenter and Allen, 1989, Chen et al., 2016, Chen et al., 2017, Fricke et al., 2019). The Monotaxinae is generally recognized as a taxonomically difficult group, mostly because of the lack of variation in meristic characters in the genus Gymnocranius (Sato, 1986, Carpenter and Allen, 1989). Despite this difficulty, four species in the genus Gymnocranius (G. obesus, G. oblongus, G. satoi and G. superciliosus) have been described within the last decade based on morphological and molecular diagnoses, and another species (Gymnocranius sp. D) has been discovered and is awaiting description (Chen et al., 2017; and references therein). Previously overseen, subtle differences in body shape and in colour patterns are of considerable interest (Chen et al., 2017). A thorough phylogeny-based revision of the subfamily is still needed to resolve the taxonomic complexity of the subfamily, to test the validity of existing species, and to possibly uncover additional hidden diversity.

Another indication of the taxonomic confusion concerning the subfamily Monotaxinae is the uncertainty in the identification of many specimens whose sequences have been deposited in public databases. As of October 2018, the BOLD and GenBank databases included 154 public records of monotaxine fishes (Supplementary Fig. S1). Among them, several specimens were identified to the genus only, some erroneously so. The COI gene haplotypes from specimens labeled “G. griseus” were positioned into four distinct clades. A similar problem was encountered with specimens labeled “G. elongatus” and “G. grandoculis” (Supplementary Fig. S1). This indicates either a high rate of misidentification, or possible mitochondrial introgression in some of the species. In any case, an in-depth investigation of the genetic relationships among species in the subfamily Monotaxinae is warranted.

While large-eye seabream species generally have a wide geographic distribution, three species are confined to a single oceanic area: G. audleyi occurs only in the western part of the Coral Sea (Carpenter and Allen, 1989); G. frenatus is found in the southern half of the Coral Triangle and the western part of the South China Sea (Carpenter and Allen, 1989); and G. obesus is currently known from the Ryukyu Islands to Bali, including Taiwan and the Flores Sea, that is, mostly the western half of the Coral Triangle (Chen et al., 2017). The central IWP as delimited in Fig. 1 in total hosts 13 of the currently known large-eye seabream species. The possible occurrence of several lineages within single species in the genus Gymnocranius in the Indian Ocean (Supplementary Fig. S1), whether resulting of misidentifications or real, deserves further scrutiny.

The main purpose of the present study is to reconstruct a complete phylogeny of the large-eye seabreams and to explore the taxonomic diversity of the subfamily, based on extensive geographic sampling of the species. We also use the reconstructed time-calibrated phylogenetic tree as a framework to infer the historical biogeography of species in the subfamily and to test whether the classical center-of-origin hypothesis, where the higher species richness of the central IWP would result from increased speciation in this central region (Briggs, 1999, Tornabene et al., 2015) may explain the spatial patterns in the distribution of monotaxine species.