Swimbladder Evolution of Longfin Herrings (Pristigasteridae, Teleostei)
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Zoological Studies 57: 39 (2018) doi:10.6620/ZS.2018.57-39 Open Access Swimbladder Evolution of Longfin Herrings (Pristigasteridae, Teleostei) Sébastien Lavoué1,5,*, Sahat Ratmuangkhwang2, Hsuan-Ching Ho3, Wei-Jen Chen1, and Mohd Nor Siti Azizah4 1Institute of Oceanography, National Taiwan University, Roosevelt Road, Taipei 10617, Taiwan 2Andaman Coastal Research Station for Development, Faculty of Fisheries, Kasetsart University, Suksamran, Ranong 85120, Thailand 3National Museum of Marine Biology and Aquarium, Pingtung 944, Taiwan 4Institute of Marine Biotechnology, Universiti Malaysia Terengganu, Kuala Nerus 21030, Malaysia 5Open Researcher and Contributor, ID: 0000-0003-4798-6666 (Received 20 April 2018; Accepted 2 July 2018; Published 31 August 2018; Communicated by Hin-Kiu Mok) Citation: Lavoué S, Ratmuangkhwang S, Ho HC, Chen WJ, Siti Azizah MN. 2018. Swimbladder evolution of longfin herrings (Pristigasteridae, Teleostei). Zool Stud 57:39. doi:10.6620/ZS.2018.57-39. Sébastien Lavoué, Sahat Ratmuangkhwang, Hsuan-Ching Ho, Wei-Jen Chen, and Mohd Nor Siti Azizah (2018) Longfin herrings form a monophyletic, circumtropically distributed family of mostly marine teleost fishes, the Pristigasteridae (Clupeoidei), that includes 38 species classified into nine genera and three main lineages (the Pelloninae, Pristigasterinae, and the genus Ilisha). The external morphology and osteology of the Pristigasteridae provide only a few, sometimes conflicting, informative characters which makes it difficult to reconstruct their phylogeny, but their swimbladder (a visceral gas-filled chamber that has several important functions in the Teleostei) appears to be highly specialized and variable among species. In particular, the swimbladder of most Indo-West Pacific pristigasterid species exhibits one or paired post-coelomic extensions, whereas New World species do not. The presence of these extensions conflicts with the current systematic classification, as they are only found in subsets of different taxa. To examine this conflict, the most comprehensive molecular phylogenetic tree of the Pristigasteridae to date was built using six molecular markers and 21 species. This tree deeply disagreed with the current classification in that it indicated that the subfamilies Pelloninae and Pristigasterinae are not monophyletic and neither are the genera Ilisha, Pellona, and Opisthopterus. Using this tree to infer the evolution of the post-coelomic extensions, it was found that their absence is the ancestral condition in the Pristigasteridae. Indo-West Pacific species with post-coelomic extensions evolved later and form a monophyletic group, inside which species with only one extension form a monophyletic group. The consequences of our findings on the evolution and classification of Pristigasteridae are discussed. We suggest that only species of Pristigasteridae having one or paired post-coelomic extensions should be included in the genus Ilisha. Key words: Evolution, Phylogeny, Morphology, Molecules, Fish. BACKGROUND not reciprocally monophyletic (Grande 1985; Whitehead 1985; Whitehead et al. 1988; Lavoué The Pristigasteridae, collectively called longfin et al. 2014). Pristigasterids are easily recognized herrings, are a small family of ray-finned fishes by their laterally compressed body, full or almost belonging to the suborder Clupeoidei (Teleostei). full series of well-developed ventral scutes, large The Clupeoidei include four additional families, eyes, reduced or absent pelvic fins, a short dorsal the Chirocentridae, Engraulidae, Clupeidae, and fin (absent in the genus Raconda), and a long Dussumieriidae, the last two of which are likely anal fin (with more than 30 fin-rays) (Whitehead *Correspondence: Tel: +886 (02) 2363 6040 ext. 408. E-mail: [email protected] © 2018 Academia Sinica, Taiwan 1 Zoological Studies 57: 39 (2018) page 2 of 13 1985). The Pristigasteridae currently comprise 38 The current phylogenetic hypothesis and species classified into nine genera (Eschmeyer et classification of the family Pristigasteridae al. 2018) and three main lineages: the subfamilies proposed by Grande (1985) (Fig. 1) need to Pristigasterinae and Pelloninae and the genus be evaluated for two reasons. First, while the Ilisha (minus I. africana, which is placed in the diagnoses for the six monospecific or species- Pristigasterinae) (Grande 1985) (Fig. 1). Three poor (≤ 3 species) genera are straightforward genera include about three-quarters of the species (Norman 1923; Berry 1964; Whitehead 1985), the diversity: Ilisha with 16 species, and Pellona and largest genus, Ilisha, which includes almost half Opisthopterus each with six species (Eschmeyer of all pristigasterid species, is poorly diagnosed et al. 2018). Two species of the Pristigasteridae because a synapomorphy is absent. Some - I. melastoma and I. elongata - are commonly authors, including Grande (1985), cast doubt about found in the northern South China Sea (Shao et al. the monophyly of Ilisha, arguing that it merely 2008), of which large (> 30 cm in standard length) represents a grade (Whitehead 1985; de Pinna specimens of I. elongata hold some economic and Di Dario 2003). However, no recent taxonomic importance in this region. revision of this genus or new hypothesis on the The monophyly of the Pristigasteridae Pristigasteridae phylogeny has been published. is supported by several morphological Second, some of the characters used by Grande synapomorphies from the structures of the gill (1985) to support clades above the level of genus arches, pre-dorsal bones, and caudal fin (Nelson either conflict with others or are absent (i.e., 1967; Grande 1985) and molecular characters the absence of the pelvic fin conflicts with the (Bloom and Lovejoy 2014), but its phylogenetic presence of post-coelomic extensions) (Fig. 1). position relative to the four other clupeoid families Whereas the external morphology and is still being debated (Grande 1985; Di Dario 2002; osteology of species of Ilisha and several other Li and Ortí 2007; Miyashita 2010; Lavoué et al. pristigasterids offer limited information regarding 2013; Bloom and Lovejoy 2014). their systematics, the morphology of their swimbladder is highly specialized and variable among species (Talwar and Whitehead 1971; Seshagiri Rao 1975, 1976; Whitehead and Blaxter 1989). The swimbladders of teleosts serve several important functions, such as regulating buoyancy or maintaining the hydrostatic position in the water column (Whitehead and Blaxter 1989; Neoopisthopterus Raconda Pliosteostoma Pellona Pristigaster other “Ilisha” Chirocentrodon “Ilisha” africana Odontognathus Opisthopterus Pelster 2011). Specialization of Pristigasteridae swimbladders may have additional purposes such as sound production, reception, or amplification e (Allen et al. 1976; Wahlberg and Westerberg 2003; a d Division A Wilson et al. 2004; Yan 2004; Wang et al. 2017), Pelloninae c Pristigasterinii although there is no direct evidence for such b functions (Whitehead and Blaxter 1989). Pristigasterinae The most striking specialization in the swimbladders of most Indo-West Pacific (IWP) 21 pristigasterid species is the one or two post- 20 Pristigasteridae coelomic extensions (Valenciennes 1847; de Beaufort 1909), which is seen as a rare condition Fig. 1. Cladogram of pristigasterid fishes based on throughout the Teleostei (Poll 1969; Tominaga et morphological characters (modified from Grande 1985). List al. 1996). In six IWP species of Ilisha (I. kampeni, of characters (reproduced from Grande, 1985): character I. lunula, I. compressa, I. melastoma, I. obfuscata, 20: “Predorsal bones oriented either vertically or inclined and I. striatula), IWP species of Opisthopterus anterodorsally”; character 21: “Loss of interlobar notch in and Raconda, and the West African I. africana, third hypural of caudal skeleton”; character a: “Maxillary- the posterior end of the swimbladder divides into premaxillary gap covered by bone”; character b: “Presence of a bony process on the first pleural rib which articulates with the two extensions (= diverticula) that pass backward shoulder girdle”; character c: “Loss of pelvic fin”; character d: on either side of the haemal spine and anal “More than 23 predorsal bones”; character e: “More than 57 pterygiophores (Fig. 2A) (Kailola 1986; Whitehead anal pterygiophores.” and Blaxter 1989; Randall 1994). The diverticula lie © 2018 Academia Sinica, Taiwan Zoological Studies 57: 39 (2018) page 3 of 13 just above the distal tips of the anal pterygiophores pristigastroides). In these species, there is only and extend to the anal fin. A second condition is one diverticulum, always on the right side of the found only in five IWP species ofIlisha (I. elongata, body (Fig. 2B). In the third and last condition, I. filigera, I. megaloptera, I. macrogaster, and I. which is the most common, the swimbladder has (A) Haemal spine sectioned Paired post-coelomic extensions (B) Haemal spine sectioned Single right post-coelomic extension (C) Ant. Post. No post-coelomic extension Horizontal section of the haemal spine Single post-coelomic extension (right side) Paired post-coelomic extensions Fig. 2. Posterior end of swimbladder showing post-coelomic diverticula. (A) Ilisha melastoma, dissected on the left side (12 cm standard length) showing the presence of two post-coelomic diverticula; (B) Ilisha elongata, dissected on the left side (42 cm standard length) showing the presence of one post-coelomic diverticulum; (C) Three diagrams (ventral view) summarizing the three conditions