Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological–molecular conflict in early vertebrate phylogeny

Abstract

SignificanceJawless, boneless, and virtually without fossil record, hagfish have long escaped systematists’ grip on their place among other fish. Yet their systematic resolution is critical to define vertebrates as a clade. Here we report an unequivocal fossil hagfish from the Cretaceous Mediterranean. Using this fossil to calibrate the evolutionary history of the group, our analysis supports hagfish and lampreys as sister groups, which likely diverged from one another in early Paleozoic times. As a result, vertebrates have a deep dichotomy, where some fossil jawless vertebrates sit closer to hagfish and lampreys than to jawed vertebrates. We showed that morphology-based analysis converged onto molecular inferences when characters are coded nonindependently, providing a case study for morphological–molecular conflicts in animal phylogeny.

A critical appraisal of appendage disparity and homology in fishes

“…Developmental studies on these extant agnathans have nonetheless provided useful information as to the evolutionary history of fish appendages. If anaspids continue to be well-supported as stem cyclostomes by future phylogenetic analyses, as suggested by Miyashita et al (2019), this would provide additional weight to the hypothesis that the paired fins found in fossil agnathans (e.g., anaspids, thelodonts) can be homologized to the paired fins of gnathostomes, as opposed to structures that have independently evolved. If anaspids continue to be well-supported as stem cyclostomes by future phylogenetic analyses, as suggested by Miyashita et al (2019), this would provide additional weight to the hypothesis that the paired fins found in fossil agnathans (e.g., anaspids, thelodonts) can be homologized to the paired fins of gnathostomes, as opposed to structures that have independently evolved.…”

“…Cyclostome monophyly was initially suggested based on morphological arguments (e.g., Schaeffer & Thomson, 1980;Yalden, 1985) and is well supported by molecular phylogenetic analyses (Delarbre, Gallut, Barriel, Janvier, & Gachelin, 2002;Furlong & Holland, 2002;Hedges, 2001;Heimberg et al, 2010;Mallatt & Sullivan, 1998;Mallatt, Sullivan, & Winchell, 2001;Stock & Whitt, 1992). However, one such recently published phylogenetic analysis incorporating a newly discovered undisputed fossil hagfish has now recovered the cyclostomes as monophyletic (Miyashita et al, 2019). However, one such recently published phylogenetic analysis incorporating a newly discovered undisputed fossil hagfish has now recovered the cyclostomes as monophyletic (Miyashita et al, 2019).…”

“…Myxines, or hagfishes, are either the most basal of extant craniates or they are basal vertebrates (see next subsection for hypothesized interrelationships among hagfishes, lampreys and gnathostomes) and comprise a single order, with about 79 extant species (Zintzen et al, 2015). Their fossil record extends at least to the Upper Carboniferous (but possibly as far as the Middle Devonian if Palaeospondylus gunni is confirmed as a primitive hagfish as suggested by Hirasawa, Oisi, & Kuratani, 2016) and includes five extinct species, three of which are only tentatively assigned to the Myxiniformes (Bardack, 1991(Bardack, , 1998Bardack & Richardson, 1977;Germain, Sanchez, Janvier, & Tafforeau, 2014;Hirasawa et al, 2016;Miyashita et al, 2019;Poplin, Sotty, & Janvier, 2001). Hagfishes have a simple fin configuration that comprises a caudal fin supported by cartilaginous fin-rays (Adam & Strahan, 1963;Ota, Fujimoto, Oisi, & Kuratani, 2011, 2013Wright, Keeley, & DeMont, 1998) and a median preanal fin-fold (Fernholm, 1998).…”

“…In contrast, analyses based on morphological data sets and incorporating fossil taxa have generally resolved 'cyclostomes' as paraphyletic relative to gnathostomes (Donoghue et al, 2000;Donoghue & Smith, 2001;Forey, 1995;Gess et al, 2006;Janvier, 1996a;Khonsari, Li, Vernier, Northcutt, & Janvier, 2009;Miyashita, 2012;Turner et al, 2010). Moreover, Miyashita et al (2019) found that anaspids and conodonts are resolved as stem cyclostomes using maximum parsimony, whereas anaspids are stem cyclostomes while conodonts are stem hagfishes using Bayesian inference. Moreover, Miyashita et al (2019) found that anaspids and conodonts are resolved as stem cyclostomes using maximum parsimony, whereas anaspids are stem cyclostomes while conodonts are stem hagfishes using Bayesian inference.…”

“…However, the affinity of Pipiscius to the petromyzontids has been questioned (Bardack, 1998;Janvier & Lund, 1983). Recent phylogenetic analyses have resolved this taxon's position either as a stem lamprey (McCoy et al, 2016;Sallan et al, 2017) or as a stem cyclostome (Miyashita et al, 2019). Furthermore, a yolk sac might be present, suggesting that Pipiscius could represent a larval organism (Bardack & Richardson, 1977).…”