Evolutionary Affinity of Billfishes (Xiphiidae and Istiophoridae) And

Molecular Phylogenetics and Evolution 56 (2010) 897–904

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Molecular Phylogenetics and Evolution

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Evolutionary affinity of billfishes (Xiphiidae and Istiophoridae) and flatfishes (Plueronectiformes): Independent and trans-subordinal origins of endothermy in teleost fishes

A.G. Little 1, S.C. Lougheed 1, C.D. Moyes *,1

Department of Biology, Queen’s University, 116 Barrie Street, Kingston, Ont., Canada K7L 3N6 article info abstract

Article history: Billfishes (Scombroidei) and tunas (Scombridae), both considered part of the suborder Scombroidei, have Received 30 September 2009 long been studied by biologists largely because of their remarkable physiological and anatomical muscu- Revised 12 April 2010 lar adaptations associated with regional endothermy and continuous swimming. These attributes, com- Accepted 16 April 2010 bined with analyses of other morphological and molecular data, have led to a general perception that Available online 21 April 2010 tunas and billfishes are close relatives, though this hypothesis has been vigorously debated. Using Bayes- ian phylogenetic analysis of nine mitochondrial and three nuclear loci (>7000 bp), we show that billfishes Keywords: are only distantly related to tunas, but rather share strong evolutionary affinities with flatfishes (Pleuro- Billfishes nectiformes) and jacks (Carangidae). This phylogenetic relationship is striking because of the marked var- Xiphiidae Istiophoridae iation in phenotype and niche across these trans-ordinal groups of fishes. Billfishes and flatfishes have Tuna each evolved radically divergent morphological and physiological features: elongated bills and extraoc- Scombridae ular heater organs in billfishes, and cranial asymmetry with complete eye migration during ontogenetic Phylogeny development in flatfishes. Despite this divergence, we identify synapomorphies consistent with the Regional endothermy hypothesis of a common billfish/flatfish/jack ancestor. Flatfishes Ó 2010 Elsevier Inc. All rights reserved. Pleuronectiformes

1. Introduction Istiophoridae, Xiphiidae, Scombridae, Sphyraenidae, Gempylidae, Trichiuridae (Johnson, 1986) and Scombrolabracidae (Collette The suborder Scombroidei (Perciformes) is a collection of tele- et al., 1984; van der Straten et al., 2006). At the center of debate ost fish, some of which share remarkable physiological adaptations surrounding scombroid phylogeny are the billfishes, comprised of related to regional endothermy (Block et al., 1993). It also includes the monotypic Xiphiidae and the monophyletic Istiophoridae (Col- some of the fastest fish in the ocean, exhibiting muscular, meta- lette et al., 2006). bolic and cardiovascular specializations for increased aerobic The phylogenetic relationships of billfishes have been explored capacities and continuous swimming (Brill, 1996; Moyes et al., in numerous morphological and molecular studies with resulting 1992). Though many scombroids share these unique features phylogenetic hypotheses differing dramatically, but more recently implying close evolutionary affinities, the taxonomic limits and edging toward classifying billfishes in their own suborder, Xiphioi- phylogenetic relationships of the group remain controversial. The dei (Finnerty and Block, 1995; Orrell et al., 2006; Collette et al., suborder has been subject to serial rearrangement (Carpenter 2006). Morphological-based phylogenies are more susceptible to et al., 1995; Collette et al., 1984; Finnerty and Block, 1995; Green- type I error because of an increased likelihood of misinterpreting wood et al., 1966; Johnson, 1986; Potthoff et al., 1980; Orrell et al., adaptive convergence (Wiens et al., 2003), but molecular data are 2006; van der Straten et al., 2006) since it was first given modern not impervious to the effects of homoplasy (Chen et al., 2003). definition by Regan in 1909 (see Carpenter et al., 1995). It has gen- Thus, even in light of new morphological evidence (Carpenter erally been accepted that Scombroidei encompasses the families et al., 1995; Johnson, 1986; van der Straten et al., 2006) and an increased breadth of molecular data (Miya et al., 2003), the greater evolutionary history of billfishes remains contentious and unresolved. * Corresponding author. Address: Department of Biology, Queen’s University, 116 Morphological studies largely support the inclusion of billfishes Barrie Street, Rm 3420, Kingston, Ont., Canada K7L 3N6. Fax: +1 613 533 6617. in Scombroidei, but tend to disagree in terms of relationships E-mail address: [email protected] (C.D. Moyes). among suborders (Fig. 1). Three general phylogenetic hypotheses 1 All three authors contributed equally to designing research, analyzing data and writing paper; A.G.L. performed laboratory work. have been supported by morphological data: that billfishes are

Fig. 1. Three differing phylogenies of scombroids and billfishes from the literature. (A) Collette et al. (1984), (B) Johnson (1986) redrawn from Fig. 1 in Finnerty and Block (1995) and (C) adapted from Orrell et al. (2006). scombroids and comprise the sister group of Scombridae (H1: plate with bases of the caudal fin rays overlapping the hypural scombrid sister group hypothesis; Collette et al., 1984), that billfishes bone; Johnson, 1986), while those supporting a non-scombroid comprise a subgroup within Scombridae (H2: scombrid subgroup hypothesis provide apparent evidence of polyphyly, citing differ- hypothesis; Carpenter et al., 1995; Johnson, 1986) and that billfish- ences in developmental and meristic characters (Nakamura, es are not scombroids and should comprise a separate suborder 1983; Potthoff et al., 1986), and sperm microstructure (van der (H3: non-scombroid hypothesis; van der Straten et al., 2006; Straten et al., 2006). If H1 or H2 are accurate, then support for Nakamura, 1983; Potthoff et al., 1986). Morphological studies sug- the H3 (non-scombroid hypothesis) can be attributed to overreli- gesting a scombroid hypothesis are supported by many seemingly ance on derived billfish features. If H3 is correct, then the traits homologous character states unique to billfishes and scombroids associated with continuous swimming in scombrids and billfish ar- (usually scombrids) such as interconnection of the gill filament ose, not from monophyly, but from convergent evolution (Finnerty blades and hypurostegy (fusion of the hypural bones into a single and Block, 1995; Nakamura, 1983). Morphological evidence to date Download English Version: https://daneshyari.com/en/article/2834587

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