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Multigene Phylogenetic Reconstruction of the Tubulinea

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Multigene Phylogenetic Reconstruction of the Tubulinea Universidade de São Paulo Biblioteca Digital da Produção Intelectual - BDPI Departamento de Zoologia - IB/BIZ Artigos e Materiais de Revistas Científicas - IB/BIZ 2013-05 Multigene Phylogenetic Reconstruction of the Tubulinea (Amoebozoa) Corroborates Four of the Six Major Lineages, while Additionally Revealing that Shell Composition Does not Predict Phylogeny in the Arcellinida Protist, Jena, v.164, n.3, p.323-339, May 2014 http://www.producao.usp.br/handle/BDPI/45007 Downloaded from: Biblioteca Digital da Produção Intelectual - BDPI, Universidade de São Paulo Protist, Vol. 164, 323–339, May 2013 http://www.elsevier.de/protis Published online date 13 March 2013 ORIGINAL PAPER Multigene Phylogenetic Reconstruction of the Tubulinea (Amoebozoa) Corroborates Four of the Six Major Lineages, while Additionally Revealing that Shell Composition Does not Predict Phylogeny in the Arcellinida a,b,1 b a,b,2 Daniel J.G. Lahr , Jessica R. Grant , and Laura A. Katz a Graduate Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts, 01003, USA b Department of Biological Sciences, Smith College, Northampton, Massachusetts, 01063, USA Submitted March 2, 2012; Accepted February 11, 2013 Monitoring Editor: Sandra L. Baldauf Tubulinea is a phylogenetically stable higher-level taxon within Amoebozoa, morphologically characterized by monoaxially streaming and cylindrical pseudopods. Contemporary phylogenetic reconstructions have largely relied on SSU rDNA, and to a lesser extent, on actin genes to reveal the relationships among these organisms. Additionally, the test (shell) forming Arcellinida, one of the most species-rich amoebozoan groups, is nested within Tubulinea and suffers from substantial under- sampling of taxa. Here, we increase taxonomic and gene sampling within the Tubulinea, characterizing molecular data for 22 taxa and six genes (SSU rDNA, actin, ␣- and ␤-tubulin, elongation factor 2 and the 14-3-3 regulatory protein). We perform concatenated phylogenetic analyses using these genes as well as approximately unbiased tests to assess evolutionary relationships within the Tubulinea. We confirm the monophyly of Tubulinea and four of the six included lineages (Echinamoeboidea, Leptomyxida, Amoebida and Poseidonida). Arcellinida and Hartmanellidae, the remaining lineages, are not mono- phyletic in our reconstructions, although statistical testing does not allow rejection of either group. We further investigate more fine-grained morphological evolution of previously defined groups, con- cluding that relationships within Arcellinida are more consistent with general test and aperture shape than with test composition. We also discuss the implications of this phylogeny for interpretations of the Precambrian fossil record of testate amoebae. © 2013 Elsevier GmbH. All rights reserved. Key words: Testate amoebae; Arcellinida; multigene phylogeny; Tubulinea; Amoebozoa. Introduction The Tubulinea are a monophyletic lineage within 1 Current Address: Department of Zoology, University of Sao the Amoebozoa (Smirnov et al. 2005). Unlike Paulo, Sao Paulo, 05508-090, Brazil 2 many other eukaryotic groups proposed in recent Corresponding author; fax +1-413 585 3786 e-mail [email protected] (D.J.G. Lahr), [email protected] years, these amoebae are marked by a puta- (L.A. Katz). tive synapomorphy (defining character): monoaxial © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.protis.2013.02.003 324 D.J.G. Lahr et al. streaming of cytoplasm within roughly cylindrical from other hartmannellids (Lahr et al. 2011). Sur- pseudopods (Smirnov et al. 2005). Some orga- prisingly, the sorocarpic (fruiting body producing) nisms in this group can produce several cylindrical slime mold Copromyxa protea was shown to be pseudopods, as in the genus Amoeba, while oth- very closely related to H. cantabrigiensis, promp- ers have a single semi-cylindrical pseudopodial ting transfer of the latter to the genus Copromyxa protrusion that comprises the entire body, giving (Brown et al. 2011). them a slug-like (limax) shape, as in the genus Arcellinida are conspicuous and abundant amoe- Saccamoeba. The Tubulinea are currently divided bae that occupy distinct tests (shells) that have into six major groups with defining morphologi- been argued to be valuable structures for both cal characteristics and varying levels of support in species delimitation and phylogenetic inference molecular reconstructions. These are: Echinamoe- (Meisterfeld 2002). In this group, molecular boidea, Leptomyxida, Amoebidae, Hartmannelli- evidence does not corroborate morphological pre- dae, Poseidonida and Arcellinida. The Tubulin- dictions in three significant and distinct instances: ida (comprised of Amoebidae + Hartmannellidae), 1) some genera appear not to be monophyletic, Echinamoeboidea, Leptomyxida and the recently including Heleopera and Nebela (Lara et al. 2008; described Poseidonida are recovered with high lev- Nikolaev et al. 2005); 2) relationships proposed els of support in trees based on SSU rDNA and based on shell form and composition are not recov- actin gene datasets (see Lahr et al. 2011). The ered – genera within the Suborder Arcellina, which Arcellinida are a species-rich assemblage char- are defined based on the possession of an organic acterized by the ability to produce a test (shell). membranous shell, are not monophyletic (e.g. Pyx- In molecular reconstructions, the Arcellinida are idicula, Arcella and Spumochlamys (Lahr et al. either not monophyletic or exhibit low to moder- 2011)), and finally; 3) at the most inclusive level, ate levels of support, with more comprehensive increased taxonomic sampling results in reduced taxon sampling tending to decrease support (Lahr support for the entire group, opening up the pos- et al. 2011; Smirnov et al. 2011). Finally, a core sibility that Arcellinida is not monophyletic (Lahr group of organisms within the Hartmannellidae are et al. 2011). However, taxonomic sampling is still often recovered with high levels of support, but far from comprehensive in this species-rich group, with the lineage Saccamoeba limax ATCC 30942 making it difficult to evaluate these taxonomic insta- branching separately from this main group, ren- bilities. dering the Hartmannellidae paraphyletic (Bolivar A further limitation of previous work is that phy- et al. 2001; Cavalier-Smith et al. 2004; Fahrni logenetic inference in the Tubulinea has relied et al. 2003; Lahr et al. 2011; Pawlowski and mostly on SSU rDNA and, to a lesser extent, on Burki 2009; Smirnov et al. 2005; Tekle et al. actin genes (Fahrni et al. 2003; Lahr et al. 2011; 2008). Smirnov et al. 2011). The problems associated with Taxonomic instability also impacts genera within single gene reconstructions are well known and the Tubulinea. The genus Hartmannella (and Fam- have been extensively dealt with elsewhere (e.g. ily Hartmannellidae by consequence) is probably Baldauf et al. 2000; Philippe and Douady 2003). one of the most affected by recent molecular The actin gene family, the second most sampled reconstructions. Many small (10-30 ␮m) amoebae marker, poses challenges for phylogenetic recon- that present a limax-like locomotive form were orig- struction due to high levels of paralogy present in inally described as different species in the genus many members of the group (Lahr et al. 2010). Hartmannella (Page 1987). Based on morpholog- Here, we present a phylogenetic reconstruction of ical evidence, several species were later removed the Tubulinea that capitalizes on sampling of SSU from the genus (e.g. Nolandella (Page 1983) and rDNA, actin and additional genes coding for four ␣ Echinamoeba (Page 1975)). Molecular studies proteins: - and ␤-tubulin, eukaryotic elongation showed that Vermamoeba vermiformis, a common factor 2 (eEF2), and the regulatory protein 14-3- freshwater and soil amoeba recently transferred out 3. We provide molecular data for 22 taxa from all of Hartmannella is in fact more closely related to six currently defined groups in the Tubulinea, with Echinamoeba than to other limax-shaped amoebae greatest emphasis on the diverse Arcellinida (15 that are now considered the “core-hartmannellids” taxa), adding a total of 111 new gene sequences. (Glaeseria, Saccamoeba) (Amaral Zettler et al. We perform phylogenetic reconstructions includ- 2000; Fahrni et al. 2003). Further, marine species ing a representative sample of eukaryotes to test of Nolandella and H. abertawensis were shown to monophyly at higher taxonomic levels, as well form the highly-supported Poseidonida (senior syn- as specific hypotheses of evolution within the onym of Nolandida (Smirnov et al. 2011)), distinct Tubulinea. Multigene Analysis of Tubulinea 325 Results monophyletic, we chose the shortest branching par- alog. Genes Characterized We characterized a total of 111 gene sequences Concatenated Trees Results for 22 taxa (Table 1): nine SSU rDNAs for seven General topology: The topology obtained from taxa (752-1958 bp), 45 actin genes from 18 taxa ∼ ␣ the concatenated analyses (Fig. 3A) is largely ( 796 bp), a total of 18 -tubulin genes for 14 congruent with comprehensive eukaryotic analy- taxa (∼900 bp), 12 ␤-tubulin genes for 10 taxa ∼ ses (e.g. Hampl et al. 2009; Parfrey et al. 2010; ( 450 bp), 9 eEF2 genes for 9 taxa and (∼840 bp), Yoon et al. 2008) and Amoebozoa-specific recons- and 15 14-3-3 genes for 10 taxa (∼500 bp). For tructions (Lahr et al. 2011; Shadwick et al. 2009; SSU rDNA, both Lesquereusia spiralis and Hele- Smirnov et al. 2005; Tekle et al. 2008). The
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