Integrating DNA and Fossils Elucidates the Evolutionary History of Hexactinellid Sponges
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Paleobiology, 39(1), 2013, pp. 95–108 Molecular paleobiology of early-branching animals: integrating DNA and fossils elucidates the evolutionary history of hexactinellid sponges Martin Dohrmann, Sergio Vargas, Dorte Janussen, Allen G. Collins, and Gert Worheide¨ Abstract.—Reconciliation of paleontological and molecular phylogenetic evidence holds great promise for a better understanding of the temporal succession of cladogenesis and character evolution, especially for taxa with a fragmentary fossil record and uncertain classification. In zoology, studies of this kind have largely been restricted to Bilateria. Hexactinellids (glass sponges) readily lend themselves to test such an approach for early-branching (non-bilaterian) animals: they have a long and rich fossil record, but for certain taxa paleontological evidence is still scarce or ambiguous. Furthermore, there is a lack of consensus for taxonomic interpretations, and discrepancies exist between neontological and paleontological classification systems. Using conservative fossil calibration constraints and the largest molecular phylogenetic data set assembled for this group, we infer divergence times of crown-group Hexactinellida in a Bayesian relaxed molecular clock framework. With some notable exceptions, our results are largely congruent with interpretations of the hexactinellid fossil record, but also indicate long periods of undocumented evolution for several groups. This study illustrates the potential of an integrated molecular/paleobiological approach to reconstructing the evolution of challenging groups of organisms. Martin Dohrmann and Sergio Vargas. Department fur¨ Geo- und Umweltwissenschaften, Ludwig-Maximilians- Universitat¨ Munchen,¨ Richard-Wagner-Strabe 10, 80333 Munich, Germany Gert Worheide.¨ Department fur¨ Geo- und Umweltwissenschaften and GeoBioCenterLMU, Ludwig-Maximilians- Universitat¨ Munchen,¨ and Bayerische Staatsammlung fur¨ Palaontologie¨ und Geologie, Richard-Wagner- Strabe 10, 80333 Munich, Germany. E-mail: [email protected]. Corresponding author. Dorte Janussen. Forschungsinstitut Senckenberg, Sektion Marine Evertebraten I, Senckenberganlage 25, 60325 Frankfurt am Main, Germany Allen G. Collins. NMFS, National Systematics Laboratory, National Museum of Natural History, MRC-153, Smithsonian Institution, Post Office Box 37012, Washington, D.C. 20013-7012, U.S.A. Accepted: 16 May 2012 Supplemental materials deposited at Dryad: doi 10.5061/dryad.sm01b Introduction Donoghue and Benton 2007; Peterson et al. The fossil record provides the only tangible 2007). Taxa vary greatly in their suitability for such evidence of the temporal distribution of taxa, integrated analyses. For diverse groups with but it is well appreciated that these data are still no appreciable fossil record, e.g., Platy- often incomplete. Furthermore, taxonomic helminthes or Placozoa, analyses integrating interpretation of fossils can be difficult when paleontological data will probably never be key characters are not preserved, leaving possible. The evolution of other important much room for speculation. Molecular se- groups for which there are only scattered quences provide an independent source of fossil occurrences, usually as partly isolated data that can be brought to bear on evolu- Lagerstatten,¨ e.g., Nematoda or Medusozoa, tionary questions. Using these data to eluci- may also be prohibitively difficult to address date the timing of evolutionary events by with synthetic analyses combining fossil and estimating dates of clade divergence, however, molecular data because first fossil occurrences requires external information, typically taken of subclades are not likely to correspond from the fossil record. Therefore, synthesizing closely to their evolutionary origin (Cart- paleontological and molecular data for a more wright and Collins 2007). A further difficulty holistic understanding of evolutionary history is posed for groups that have a relatively rich is one of the most promising—and most fossil record, but whose phylogenetic histories challenging—lines of modern paleobiological are difficult to reconstruct with morphological research (Brochu et al. 2004; Magallon´ 2004; data owing to the paucity of informative Ó 2013 The Paleontological Society. All rights reserved. 0094-8373/13/3901-0006/$1.00 96 MARTIN DOHRMANN ET AL. characters and high levels of homoplasy. evidence, thereby coming to an enhanced Sponges (Porifera) are perhaps the most appreciation of hexactinellid evolution. notorious example of such a taxon (see Fossil Record and Systematics of Glass Spong- Hooper and van Soest 2002; Ca´rdenas et al. es.—Hexactinellids were important compo- 2012). Although molecular systematics has nents of deep- and at times also shallower- greatly helped resolve relationships of extant water benthic ecosystems throughout the sponges (Erpenbeck and Worheide¨ 2007; Phanerozoic, often associated with reef com- Worheide¨ et al. 2012), it has also generally munities (e.g., Finks 1960; Mehl 1992; Brunton indicated that traditional sponge classification and Dixon 1994; Leinfelder et al. 1994; and taxonomy is based on characters that do Krautter et al. 2001; Carrera and Botting not accurately reflect evolutionary history 2008). Their rich fossil record (see Krautter (Ca´rdenas et al. 2012). Morphology-based 2002; Pisera 2006) dates back to the late classification, which is already difficult for Neoproterozoic (Steiner et al. 1993; Gehling extant taxa, is thus even more problematic for and Rigby 1996; Brasier et al. 1997). The two fossil sponges. Paleontologists naturally have extant subclasses, Hexasterophora and Am- to rely on morphological characters for taxo- phidiscophora, whose monophyly is strongly nomic assignment, and the task for sponges is supported by both morphological and molec- complicated by a fossil record biased toward ular data (Mehl 1992; Dohrmann et al. 2008), groups with fused or articulated skeletons, appear in the early Paleozoic, as indicated by leaving substantial gaps for taxa that more isolated microscleres (Mostler 1986). Because readily disintegrate after death (Pisera 2006). the oldest hexasters (the defining autapomor- This difficult situation, however, is less severe phy of Hexasterophora) are known from the in the Hexactinellida (glass sponges), which lowermost Ordovician, the hexasterophoran have recently been shown to have an evolu- and amphidiscophoran stem-lineages must tionary history, as elucidated by molecular have already evolved during the Cambrian sequence data, that is largely consistent with (Mostler 1986; Mehl 1996). However, given the distribution of morphological features that the earliest (late Ediacaran and early across its traditional taxa (Dohrmann et al. Cambrian) bodily preserved hexactinellid fos- 2008, 2009). However, the fossil record pres- sils (e.g., Steiner et al. 1993; Gehling and Rigby ently provides incomplete or ambiguous 1996; Brasier et al. 1997; Wu et al. 2005; Xiao et evidence regarding the origin and evolution al. 2005) bear no resemblance to any specific of extant hexactinellid subtaxa (see next extant subtaxon, it is likely that they represent section). Furthermore, the poor concordance stem-group members, implying that the origin between paleontological and neontological of the crown group (i.e., the split between the systematics greatly complicates matters two subclasses) does not predate the Ediacar- (Krautter 2002; Reiswig 2006). an/Cambrian boundary. Thus, although the Here we use glass sponges to illustrate how origin of Hexactinellida from a common a molecular paleobiological approach (Peter- ancestor with demosponges certainly occurred son et al. 2007) can enhance our understand- in Precambrian times, their crown group likely ing of the evolution of such ‘‘problematic’’ evolved rapidly as part of the Cambrian animal groups. We estimate divergence times radiation (see Zhang and Pratt 1994; Reitner of crown-group Hexactinellida from the larg- and Mehl 1995; Xiao et al. 2005; see also Erwin est molecular phylogenetic data set assembled 2011). to date for this class of sponges (Dohrmann et Following a high Paleozoic diversity, most al. 2012a), using a relaxed molecular clock groups dominant in that era had disappeared approach (see, e.g., Welch and Bromham 2005; by the end of the Permian (Mostler 1990; Mehl Yang 2006 for reviews) and fossil-based age 1996; Mehl-Janussen 1999; Krautter 2002). constraints for calibration. We then compare Because the taxonomically important micro- the dated phylogeny with the fossil record and scleres are rarely preserved in situ (but see, discussimplicationsofcongruenciesand e.g., Kling and Reif 1969 and Rigby et al. 2007 discrepancies between the two sources of for notable exceptions), and Paleozoic skeletal MOLECULAR PALEOBIOLOGY OF HEXACTINELLIDA 97 architectures differ greatly from Mesozoic and majority of hexactinosidans form a highly modern forms (Mehl and Mostler 1993; Mehl supported clade, the Sceptrulophora (Mehl 1996), relationships of these taxa to extant 1992; Dohrmann et al. 2011), which is the sister hexactinellids remain largely elusive. Thus, group of the remaining hexasterophorans fossils assigned to modern families are mostly (Dohrmann et al. 2008, 2009). This taxon is confined to the Mesozoic–Cenozoic. The fossil characterized by the possession of sceptrules, record of Amphidiscophora is poor (Mehl a scepter-like spicule type that occurs in 1992, 1996), and the earliest crown-group various forms, mostly scopules or clavules member (family Hyalonematidae)