Phylogenomics supports Panpulmonata: Opisthobranch paraphyly and key evolutionary steps in a major radiation of gastropod molluscs

Molecular Phylogenetics and Evolution

Volumn 69, Issue 3, 2013, Pages 764-771

  Kocot, Kevin M ^a   Halanych, Kenneth M ^a   Krug, Patrick J ^b  

^a AUBURN UNIVERSITY   (United States)

^b CALIFORNIA STATE UNIVERSITY   (United States)

Author keywords

Gastropoda; Heterobranch; Opisthobranch; Phylogenomics; Pulmonate; Radiation

Indexed keywords

ANIMALIA; ARTHROPODA; BASOMMATOPHORA; GASTROPODA; MOLLUSCA; OPISTHOBRANCHIA; PULMONATA; SACOGLOSSA; SIPHONARIOIDEA;

MITOCHONDRIAL DNA; RIBOSOME DNA; TRANSCRIPTOME;

ANIMAL; ARTICLE; BAYES THEOREM; BIOLOGICAL MODEL; CELL NUCLEUS; CLASSIFICATION; DNA SEQUENCE; EVOLUTION; GASTROPOD; GENETICS; HETEROBRANCH; OPISTHOBRANCH; PHYLOGENOMICS; PHYLOGENY; PULMONATE; RADIATION; STATISTICAL MODEL;

GASTROPODA; HETEROBRANCH; OPISTHOBRANCH; PHYLOGENOMICS; PULMONATE; RADIATION;

ANIMALS; BAYES THEOREM; BIOLOGICAL EVOLUTION; CELL NUCLEUS; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL; GASTROPODA; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; PHYLOGENY; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

EID: 84884588985     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2013.07.001     Document Type: Article

References (53)

1. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
2. Chou H.-H., Holmes M.H. DNA sequence quality trimming and vector removal. Bioinformatics 2001, 17:1093-1104.
3. Dayrat B., Conrad M., Balayan S., White T.R., Albrecht C., Golding R., Gomes S.R., Harasewych M.G., Frias De., Martins A.M. Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): new insights from increased taxon sampling. Mol. Phylogenet. Evol. 2011, 59:425-437.
4. Dayrat B., Tillier S. Evolutionary relationships of euthyneuran gastropods (Mollusca): a cladistic re-evaluation of morphological characters. Zool. J. Linnean Soc. 2002, 135:403-470.
5. DeVilliers C.J., Hodgson A.N. The structure of the secondary gills of Siphonaria capensis (Pulmonata: Gastropoda). J. Mollusc. Stud. 1987, 53:129-138.
6. Dieuzeide, R., 1935. Contribution à l'étude de deux types de Gastéropodes Pulmonés Marins: Siphonaria algesirae, Gadinia garnoti. Thesis. Bordeaux: Université de Bordeaux.
7. Dinapoli A., Klussmann-Kolb A. The long way to diversity - phylogeny and evolution of the Heterobranchia (Mollusca: Gastropoda). Mol. Phylogenet. Evol. 2010, 55:60-76.
8. Douady C.J., Delsuc F., Boucher Y., Doolittle W.F., Douzery E.J.P. Comparison of Bayesian and Maximum Likelihood bootstrap measures of phylogenetic reliability. Mol. Biol. Evol. 2003, 20:248-254.
9. Forment J., Gilabert F., Robles A., Conejero V., Nuez F., Blanca J. EST2uni: an open, parallel tool for automated EST analysis and database creation, with a data mining web interface and microarray expression data integration. BMC Bioinformatics 2008, 9:5.
10. Gascoigne T. The reproductive systems and classification of the Stiligeridae (Opisthobranchia: Sacoglossa). J. Malac. Soc. Aust. 1976, 3:157-172.
11. Grande C., Templado J., Zardoya R. Evolution of gastropod mitochondrial genome arrangements. BMC Evol. Biol. 2008, 8:61.
12. Händeler K., Grzymbowski Y.P., Krug P.J., Wägele H. Functional chloroplasts in metazoan cells - a unique evolutionary strategy in animal life. Front. Zool. 2009, 6:28.
13. Haszprunar G. The Heterobranchia - a new concept of the phylogeny of the higher Gastropoda. J. Zool. Syst. Evol. Res. 1985, 23:15-37.
14. Haszprunar G. On the origin and evolution of major gastropod groups, with special reference to the Streptoneura. J. Mollus. Stud. 1988, 54:367-441.
15. Hodgson, A.N., 1999. The biology of siphonariid limpets (Gastropoda: Pulmonata). In: Gibson, R.N. (Ed.) Ann. Rev. Oceanogr. Mar. Biol., vol. 37, pp. 245-314.
16. Huang X., Madan A. CAP3: A DNA Sequence Assembly Program. Genome Res. 1999, 9:868-877.
17. Huelsenbeck J.P., Rannala B. Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst. Biol. 2004, 53:904-913.
18. Hyman L.H. Mollusca. The Invertebrates 1967, 1-792. MacGraw-Hill Co., New York. L.H. Hyman (Ed.).
19. Jörger K., Stoger I., Kano Y., Fukuda H., Knebelsberger T., Schrodl M. On the origin of Acochlidia and other enigmatic euthyneuran gastropods, with implications for the systematics of Heterobranchia. BMC Evol. Biol. 2010, 10:323.
20. Katoh K., Kuma K., Toh H., Miyata T. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005, 33:511-518.
21. Klussmann-Kolb A., Dinapoli A., Kuhn K., Streit B., Albrecht C. From sea to land and beyond - New insights into the evolution of euthyneuran Gastropoda (Mollusca). BMC Evol. Biol. 2008, 8:57.
22. Kocot K.M., Cannon J.T., Todt C., Citarella M.R., Kohn A.B., Meyer A., Santos S.R., Schander C., Moroz L.L., Lieb B., Halanych K.M. Phylogenomics reveals deep molluscan relationships. Nature 2011, 477:452-456.
23. Kück P., Meusemann K., Dambach J., Thormann B., Von Reumont B.M., Wägele J.W., Misof B. Parametric and non-parametric masking of randomness in sequence alignments can be improved and leads to better resolved trees. Front. Zool. 2010, 7:1-12.
24. Lartillot N., Philippe H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 2004, 21:1095-1109.
25. Lartillot N., Lepage T., Blanquart S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 2009, 25:2286.
26. Li L., Stoeckert C.J., Roos D.S. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res. 2003, 13:2178-2189.
27. Lottaz C., Iseli C., Jongeneel C.V., Bucher P. Modeling sequencing errors by combining Hidden Markov models. Bioinformatics 2003, 19:ii103-ii112.
28. Lydeard C., Cowie R.H., Ponder W.F., Bogan A.E., Bouchet P., Clark S.A., Cummings K.S., Frest T.J., Gargominy O., Herbert D.G., Hershler R., Perez K.E., Roth B., Seddon M., Strong E.E., Thompson F.G. The global decline of nonmarine mollusks. BioScience 2004, 54:321-330.
29. Marcus Ev., Marcus Er. On Siphonaria hispida. Universidade de São Paulo. Faculdade de Filosofia, Ciências e Letras. Boletim de Zoologia 1960, 23:107-139.
30. Medina M., Lal S., Vallès Y., Takaoka T.L., Dayrat B.A., Boore J.L., Gosliner T. Crawling through time: transition of snails to slugs dating back to the Paleozoic, based on mitochondrial phylogenomics. Mar. Genomics 2011, 4:51-59.
31. Mikkelsen P.M. The evolutionary relationships of Cephalaspidea S.L. (Gastropoda: Opisthobranchia): a phylogenetic analysis. Malacologia 1996, 37:375-442.
32. Mikkelsen P.M. Cylindrobulla and Ascobulla in the western Atlantic (Gastropoda, Opisthobranchia, Sacoglossa): systematic review, description of a new species, and phylogenetic reanalysis. Zool. Scripta 1998, 27:49-71.
33. Misof B., Misof K. A Monte Carlo approach successfully identifies randomness in multiple sequence alignments: a more objective means of data exclusion. Syst. Biol. 2009, 58:21-34.
34. Mordan, P., Wade, C., 2008. Heterobranchia II: The Pulmonata., Phylogeny and evolution of the Mollusca. In: Ponder, W.F., Lindberg, D.R. (Eds.), University of California Press, Berkeley and Los Angeles, CA, pp. 409-426.
35. Morton J.E. The functional morphology of Otina otis, a primitive marine pulmonate. J. Mar. Biol. Assoc. UK 1955, 34:113-150.
36. Morton J.E. The form and functioning of the pallial organs in the opisthobranch Akera bullata with a discussion on the nature of the gill in Notaspidea and other tectibranchs. Veliger 1972, 14:337-349.
37. Pierce S.K., Curtis N.E. The cell biology of the chloroplast symbiosis in sacoglossan sea slugs. Int. Rev. Cell. Mol. Biol. 2012, 293:123-148.
38. Pierce S.K., Fang X., Schwartz J.A., Jiang X., Zhao W., Curtis N.E., Kocot K.M., Yang B., Wang J. Transcriptomic evidence for the expression of horizontally transferred algal nuclear genes in the photosynthetic sea slug, Elysia chlorotica. Mol. Biol. Evol. 2012, 29:1545-1556.
39. Price M.N., Dehal P.S., Arkin A.P. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE 2010, 5:e9490.
40. Ruthensteiner B. Homology of the pallial and pulmonary cavity of gastropods. J. Molluscan Stud. 1997, 63:353-367.
41. Schrödl M., Jörger K.M., Klussman-Kolb A., Wilson N.G. Bye bye "Opisthobranchia"! A review on the contribution of mesopsammic sea slugs to euthyneuran systematics. Thalassas 2011, 27:101-112.
42. Schrödl M., Jörger K.M., Wilson N.G. A reply to Medina et al. (2011): Crawling through time: Transition of snails to slugs dating back to the Paleozoic based on mitochondrial phylogenomics. Mar. Genomics 2011, 4:301-303.
43. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 2002, 51:492-508.
44. Smith S.A., Wilson N.G., Goetz F.E., Feehery C., Andrade S.C.S., Rouse G.W., Giribet G., Dunn C.W. Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature 2011, 480:364-367.
45. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688.
46. Stöger, I., Schrödl, M., 2013. Mitogenomics does not resolve deep molluscan relationships (yet?). Mol. Phylog. Evol. (in press). http://dx.doi.org/10.1016/j.ympev.2012.11.017.
47. Strong E., Gargominy O., Ponder W., Bouchet P. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia 2008, 595:149-166.
48. Vinther J., Sperling E.A., Briggs D.E.G., Peterson K.J. A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors. Proc. R. Soc. Lond. 2011, 279:1259-1268.
49. Wägele H., Deusch O., Händeler K., Martin R., Schmitt V., Christa G., Pinzger B., Gould S.B., Dagan T., Klussmann-Kolb A., Martin W. Transcriptomic evidence that Longevity of acquired plastids in the photosynthetic slugs Elysia timida and Plakobranchus ocellatus does not entail lateral transfer of algal nuclear genes. Mol. Biol. Evol. 2011, 28:699-706.
50. Wägele H., Klussmann-Kolb A. Opisthobranchia (Mollusca, Gastropoda) - more than just slimy slugs. Shell reduction and its implications on defence and foraging. Front. Zool. 2005, 2:1-18.
51. Wägele H., Willan R. Phylogeny of the nudibranchia. Zool. J. Linn. Soc. 2000, 130:83-181.
52. White T.R., Conrad M.M., Tseng R., Balayan S., Golding R., Martins A.M.de F., Dayrat B.A. Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships. BMC Evol. Biol. 2011, 11:295.
53. Yonge C.M. The mantle cavity in Siphonaria alternata Say. Proc. Malacol. Soc. Lond. 1952, 29:190-199.