Polar Biology https://doi.org/10.1007/s00300-019-02489-1 ORIGINAL PAPER Recent diversifcation in an ancient lineage of Notothenioid fshes (Bovichtus: Notothenioidei) Thomas J. Near1,2 · Ava Ghezelayagh1 · F. Patricio Ojeda3 · Alex Dornburg4 Received: 3 August 2018 / Revised: 24 February 2019 / Accepted: 13 March 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Notothenioids are among the most intensively studied lineages of marine fshes. However, notothenioid research is pre- dominately focused on the approximately 100 species of Antarctic cryonotothenioids. Far less attention is devoted to the non-Antarctic lineages Bovichtidae, Pseudaphritis urvillii, and Eleginops maclovinus, all of which originated prior to the diversifcation of cryonotothenioid species. Here we utilize DNA sequence data from mitochondrial and nuclear genes, as well as meristic trait morphology to investigate the evolutionary history of Bovichtidae. Bovichtus is the only polytypic lineage of early diverging non-Antarctic notothenioids providing a unique opportunity to contextualize the diversifcation dynamics of cryonotothenioids with their non-Antarctic relatives. We fnd strong evidence that species of Bovichtus represent a recent evolutionary radiation with divergence times similar to those estimated among the most closely related species of cryonotothenioids. The divergence in traditional meristic trait morphology among species of Bovichtus is consistent with their phylogenetic relationships. The phylogeny of Bovichtus implies the wide geographic distribution of species in the clade is likely the result of West Wind drift-driven dispersal. The phylogeny and divergence time estimates results reject a hypothesis that species persistence in Bovichtus refects long periods of evolutionary stasis. Instead, we hypothesize that patterns of extinction and diversifcation in Bovichtus closely mirror those observed in their Antarctic relatives. Keywords West Wind drift · Historical biogeography · Notothenioidei · Bovichtidae · Adaptive radiation Introduction Kock 1985; Barrera-Oro 2002; La Mesa et al. 2004), and are considered a rare example of adaptive radiations among Notothenioids, which dominate the near-shore marine habi- marine fshes (Clarke and Johnston 1996; Near et al. 2012). tats of the Southern Ocean, are one of the most intensively Although important advances in understanding the evolu- studied lineages of teleost fshes (Cheng and Detrich 2007). tionary history and ecology of Antarctic notothenioids have This attention is not unwarranted as notothenioids are of developed over the past 25 years (Eastman 1993; Bargelloni critical importance to multi-national fshing interests (Kock et al. 2000; Near et al. 2012, 2018; Dornburg et al. 2017), far 1992; Collins 2010), are a key component of the marine food less attention has been devoted toward the development of web dynamics of the Southern Ocean (Eastman 1985a, b; an evolutionary framework that focuses on the non-Antarctic lineages Bovichtidae, Pseudaphritis urvillii, and Eleginops maclovinus (Near et al. 2015; Papetti et al. 2016). As result, * Thomas J. Near [email protected] there is no perspective to compare diversifcation dynamics of the Antarctic adaptive radiation with other notothenioid 1 Department of Ecology and Evolutionary Biology, Osborn lineages. Memorial Labs, Yale University, P.O. Box 208106, A notable feature of notothenioid phylogenetic diversity New Haven, CT 06520-8106, USA is the presence of non-Antarctic species-depauperate lin- 2 Peabody Museum of Natural History, Yale University, eages, Bovichtidae (6 species), Pseudaphritis urvillii, and New Haven, CT 06520-8106, USA Eleginops maclovinus that form successive sister lineages 3 Departamento de Ecología, Facultad de Ciencias Biológicas, of the predominantly Antarctic Cryonotothenioidea (Fig. 1). Pontifcia Universidad Católica de Chile, Santiago, Chile The divergences times of Bovichtidae and Pseudaphritis 4 North Carolina Museum of Natural Sciences, Raleigh, are consistently placed in the Cretaceous (Near 2004, 2009; NC 27601, USA Vol.:(0123456789)1 3 Polar Biology Fig. 1 Current phylogenetic hypothesis of early diverging notothenioid relationships as discussed in the text. Diver- gence times refect those esti- mated in Near et al. (2015) Near et al. 2012, 2015), with their origins hypothesized to informed perspective on species diversity, the current lack have resulted from continental fragmentation in the Southern of a phylogenetic hypothesis challenges the development of Hemisphere (DeWitt 1971; Miller 1987; Balushkin 2000; a more robust understanding of the evolutionary history of Near et al. 2015). Given that no fossils have been found for Bovichtus. these lineages and that both Cottoperca and Pseudaphri- Collectively, the six recognized species of Bovichtus tis are monotypic, investigating the evolutionary history of are widely distributed (Fig. 2) from the Pacifc and Atlan- Bovichtus represents the only opportunity to explore pat- tic coasts of southern South American, the Antarctic Pen- terns of speciation in a polytypic ancestrally non-Antarctic insula, Tristan da Cunha, St. Paul Island in the southern notothenioid clade. Inference of a species-level phylogeny Indian Ocean, southern Australia and Tasmania, New Zea- for Bovichtus has never been attempted (Papetti et al. 2016). land, the Campbell Plateau, and seamounts east of New Molecular phylogenetic analyzes that include Bovichtus Zealand in the southern Pacifc (Sauvage 1879; Hureau and have only included two species, B. variegatus and B. dia- Tomo 1977; Hardy 1988; Kingsford et al. 1989; Andrew canthus, which resolve as monophyletic with strong node et al. 1995; Bravo et al. 1999; Balushkin 2016). Relaxed support (Near et al. 2012). All other systematic investiga- molecular clock analyzes have consistently estimated an age tions of Bovichtus have used meristic and morphometric for most recent common ancestor (MRCA) of Bovichtidae traits to assess the distinctiveness of the described species. (Cottoperca trigloides and Bovichtus) at ~ 40 Myr. This is Regan (1913, pp. 255–257) reviewed eight species of Bovi- nearly twice the age ( ~ 23 myr) estimated for the MRCA of chtus, providing descriptions of B. angustifrons, B. chilen- the species-rich Cryonotothenioidea (Near et al. 2012, 2015; sis, and B. decipiens. Comparison of meristic data taken Dornburg et al. 2017). Given this ancient divergence time from a large number of specimens resulted in B. argentinus between Cottoperca trigloides and Bovichtus (Fig. 1), it is Mac Donagh and B. elongatus Hureau and Tomo being syn- not clear if the wide geographic distribution of Bovichtus is onymized with B. chilensis (Bravo et al. 1999). In a review the result of speciation events that occurred in the Paleogene of the Australasian species of Bovichtus, B. oculus Hardy and the living diversity of Bovichtus is the result of a grad- was described from a single specimen, B. decipiens and B. ual accumulation of lineages through time. Alternatively, if roseopictus Hutton were synonymized with B. variegatus the timing of diversifcation in Bovichtus is more recent, it Richardson, and Aurion efulgens Waite was synonymized suggests similar patterns of lineage diversifcation that are with B. psychrolutes Gunther (Hardy 1988). A recent study observed among species of Antarctic distributed Cryono- by Balushkin (2016) led to the additional reduction of the tothenioidea (Stankovic et al. 2002; Near et al. 2012; Hüne number recognized species of Bovichtus by synonymizing B. et al. 2015; Dornburg et al. 2017). The absence of a molecu- oculus with B. psychrolutes. While these studies provide an lar time tree has precluded investigating the evolutionary 1 3 Polar Biology Fig. 2 Map showing the geo- graphic distribution of the six recognized species of Bovichtus history and timing of diversifcation in Bovichtus. Over the Phylogenies were inferred from each of the fve sampled past 20 years, we have been able to gather specimens from genes using MrBayes v. 3.2 (Ronquist et al. 2012). For each four of the six recognized species of Bovichtus for molecular nuclear gene, an HKY substitution model was applied and a phylogenetic analysis. In this study, we investigate the phy- GTR + Γ4 model was used for the mitochondrial ND2 gene logenetic relationships within Bovichtus and timing of diver- based on Akaike information criterion-based model selec- sifcation in the lineage using a dataset of DNA sequences tion in ModelTest (Posada and Crandall 1998). The MrBayes from mitochondrial and nuclear genes. v. 3.2 analysis was run for 107 generations with two simul- taneous runs each with four chains. Convergence and sta- tionarity of the chains were assessed through visual inspec- tion of the chain likelihoods and by monitoring the average Materials and methods standard deviation of the split frequencies between the two runs, which was less than 0.005 after 2 × 106 generations. Tissue samples were obtained from specimens collected The frst 50% of the sampled generations were discarded as during several expeditions, and most of these specimens burn-in, and the posterior phylogeny was summarized as a are maintained in museum research collections (Table 1). 50% majority-rule consensus tree. Qiagen DNeasy Blood and Tissue kits were used to iso- We jointly estimated divergence times and the tree topol- late DNA from frozen or ethanol preserved muscle tissues. ogy for early diverging notothenioids using a multispe- Four nuclear genes (enc1,