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Implications from a 28Srdna Tree UvA-DARE (Digital Academic Repository) On the Phylogeny of Halichondrid Demosponges Erpenbeck, D.J.G. Publication date 2004 Link to publication Citation for published version (APA): Erpenbeck, D. J. G. (2004). On the Phylogeny of Halichondrid Demosponges. Universiteit van Amsterdam. General rights It is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an open content license (like Creative Commons). Disclaimer/Complaints regulations If you believe that digital publication of certain material infringes any of your rights or (privacy) interests, please let the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the material inaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letter to: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. You will be contacted as soon as possible. UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl) Download date:30 Sep 2021 Chapterr 3 Phylogeneticc relationships of halichondrid demosponges Implicationss from a 28SrDNA tree Erpenbeckk D., Breeuwer J.A.J, and R.W.M. van Soest Abstract t Halichondridaa is a pivotal demosponge order of which the classification underwent major changes inn the recent history. The monophyly of Halichondrida and its intra-ordinal phylogeny cannot be reliablyy determined on the basis of morphology. Here, we present a 28SrDNA gene tree of selected halichondrids,, which supports the hypothesis of halichondrid non-monophyly and elucidates furtherr inter-ordinal relationships: Most Halichondrid families (Axinellidae, Dictyonellidae and Halichondriidae)) are polyphyletic and the molecular classification of certain genera such as Axinyssa andd Stylissa do not agree with the current (morphological) system. 47 7 3:: Phylogcnetic relationships of halichondrid demosponges - Implications from a 28SrDNA tree Introduction n Thee phylogenetic systematics of the demosponge order Halichondrida is pivotal in demosponge systematicss as its composition and affinities in history reflect the major changes in demosponge systematicss that were proposed in the second half of the 20th century. Grayy (1867) erected the taxon "Halichondriadae". Its composition was modified based onn morphological features by Vosmaer (1886 [1887]), Ridley and Dendy (1887) Topsent (1928) andd de Laubenfels (1936). Later, a new demosponge classification was founded by Levi (1953), entirelyy based on reproductive features. Demosponges were divided in two major subclasses 'Tetractinomorpha'' (oviparous taxa) and 'Ceractionomorpha' (viviparous taxa) as these features matchedd with large demosponge groups and resulted in a reallocation of formerly recognized orders andd families in separate clades. The order Halichondrida sensu Laubenfels (1936) was split up in the ceractinomorphh "Halichondrida s.s." (including the currently recognized families Halichondriidae andd Dictyonellidae) and the tetractinomorph "Axinellida" (including the currently recognized familiess Axinellidae, Desmoxyidae and Bubaridae). Levi's classification was elaborated by Bergquist (e.g.,, 1980) and Hartman (1982). It formed the backbone of demosponge systematics in the second halff of the 20th century. Withh the introduction of cladistic character analyses in sponge systematics (Van Soest, 1985) parsimony-inconsistenciess of Levi's classification were criticized (Van Soest, 1987; Hooper, 1990). Evidencee for a paraphyletic nature of the two major demosponge subclasses could be shown and an alternativee classification was suggested (Van Soest, 1991) which gained broader acceptance in the recentt years (Levi, 1997). The taxon Axinellida sensu Levi was abandoned and partially (Axinellidae andd Desmoxyidae) merged with Halichondrida (Van Soest et al, 1990). Van Soest and Hooper (2002)) currently assign the families Halichondriidae, Dictyonellidae, Desmoxyidae, Bubaridae, andd Axinellidae to this order. However, until now not a single morphological synapomorphy, whichh could define the families as monophyletic units, has been described, nor synapomorphies, whichh could unite the families to a monophyletic taxon Halichondrida. The order is still defined by characterr combinations and underlying synapomorphies, which results in the fact, that intra-ordinal phylogeneticc relationships of this pivotal demosponge taxon are not properly resolved. In particular the familyy Dictyonellidae sensu Van Soest et al., (2002) is rather based on assumed secondary losses than onn observable characters. Van Soest et al. (1990) proposed a phylogeny for the order and the family Halichondriidaee based on distribution of morphological characters, but did not present statistical support.. The erection of a comprehensive cladistically supported phylogeny of the Halichondrida is hamperedd (as for many other demosponge taxa) by either the lack of phylogenetically informative characterss and diverging views of their interpretation (Carballo et al., 1996). To gain additional characterss in sponge systematics, cytological features (Boury-Esnault et al., 1994) as well as chemical compounds,, e.g., Van Soest and Braekman (1999) have been recruited but these approaches suffer untill now from a taxon bias and ambiguities in pathway homology and metabolite origin (sponge or symbiont?). Thee main progress in recent sponge systematics lies in the gain of DNA sequence data. The largee subunit of the cytoplasmatic ribosome (28SrDNA) frequently has been used to reconstruct phylogeneticc trees (Alvarez et al., 2002; McCormack and Kelly, 2002) although several other sponge geness have recently been sequenced (an overview in Borchiellini et al., 2000). Somee of these 28SrDNA analyses yielded evidence against a monophyletic relationship of thee halichondrids sensu Van Soest et al. (1990). One analysis of the C1-D2 region found the family 48 8 3:: Phylogenetic relationships of halichondrid demosponges - Implications from a 28SrDNA tree Halichondriidaee in a shared clade with the hadromerid family Suberitidae (Chombard and Boury- Esnault,, 1999). The resulting taxon, called "Suberitina" still lacks acceptance as it fails to show unambiguouss morphological synapomorphies notably regarding the spicule geometry. McCormack andd Kelly (2002) analyzed the D3-D5 region of the 28SrDNA molecule to unravel the phylogenetic positionn of the hermit-crab sponge Spongosorites suberitoides. Their resulting tree favored a close relationshipp of the halichondrid genus Topsentia (Halichondriidae) with the hadromerid genus Tethya (Tethyidae)) and additionally Hymeniacidon (Halichondrida: Halichondriidae) with Aaptos and SuberitesSuberites (Hadromerida: Suberitidae), which increased molecular evidence for close Halichondrid- Hadromeridd relationships. Furtherr 28SrDNA studies (Lafay et al., 1992; Chombard et al., 1997; Alvarez et al., 2000) foundd a close relationship of species of the order Agelasida {Agelas) with axinellid halichondrids {Axinella).{Axinella). Such an Agelas I Axinella clade can only be explained morphologically with multiple aa priori assumed analogies, but it finds support in chemical analyses by the common possession of chemicall compounds of the pyrrole-2-carboxylic acid family (Braekman et al., 1992; Van Soest and Braekman,, 1999) and glycosyl ceramides (Costantino et al., 1996). Alll these analyses comprised only a subset of halichondrids and made a comprehensive studyy of halichondrids of all families necessary to elucidate its composition and relationships to non-halichondrids.. In mis study we present a subsequent comprehensive 28SrDNA study from the Halichondridd perspective. Erpenbeck et al. {submitted, Chapter 2) observed that the 28S gene structure inn sponges underlies differences on order level. Based on those findings we could narrow down the taxonn set to a homogeneous and comparable character set without long branches which might mask phylogeneticc information and lead to an erroneous signal. Here, we present the results of a combined taxonn set based on the 28 S D3-D5 region, which unites representative Halichondrida with Agelasida andd certain Hadromerida. In order to test in an enlarged taxon set for the monophyly of Halichondrida sensuu Van Soest et al. (1990) and to get insight in phylogenetic relationships between and inside their families.. We test the existence of a "Suberitina" clade as proposed by Chombard et al. (1997) in this enlargedd taxon set with a different 28SrDNA fragment. Materiall and Methods Thee sponge tissue was either freshly collected with SCUBA diving, or sampled during the SYMBIOSPONGEE project (EU-MAS3CT 97-0144). A complete list of species studied is given in Tab.. 1. Up to three specimens per species were examined. DNA extraction and PCR setup, cloning andd sequencing was carried out as described in Erpenbeck et al. (2002). PCR primers employed weree taken from McCormack and Kelly, (2002, primers: RD3A: GACCCGTCTTGAAACACGA andd RD5B2: (ACACACTCCTTAGCGGA, temperature regime: 94° 3min during which the Taq polymerasee is added, 35x (94° 30s; 50° 20s; 72° 60s), 72° lOmin). The new sequences are submitted too Genbank. Sequencee management was performed using MacClade 4.03 (Maddison and Maddison, 1992).. DAMBE (Xia and Xie, 2001) was used to fetch and splice the sequences from Genbank (http://www.ncbi.nlm.nih.gov/))
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