Systematic Biology Advance Access originally published online on August 21, 2009
Systematic Biology 2009 58(5):509-526; doi:10.1093/sysbio/syp044
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Molecular Phylogenetics of Thecata (Hydrozoa, Cnidaria) Reveals Long-Term Maintenance of Life History Traits despite High Frequency of Recent Character Changes
1 Université Paris 06, UMR 7138 CNRS UPMC MNHN IRD, 7 quai St Bernard, Case 05, Batiment A, 4ème étage, 75005 Paris, France
2 Muséum d'histoire naturelle, CP 6434, CH-1211 Genève 6, Switzerland
3 Genoscope. Centre National de Séquençage. 2, rue Gaston Crémieux, CP5706, 91057 Evry Cedex, France
* Correspondence to be sent to: Université Paris 06, UMR 7138 CNRS UPMC MNHN IRD, 7 quai Saint Bernard, Case 05, Bâtiment A, 4ème étage, 75252 Paris Cedex 05, France; E-mail: lucas.leclere{at}snv.jussieu.fr.
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Abstract |
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Two fundamental life cycle types are recognized among hydrozoan cnidarians, the benthic (generally colonial) polyp stage either producing pelagic sexual medusae or directly releasing gametes elaborated from an attached gonophore. The existence of intermediate forms, with polyps producing simple medusoids, has been classically considered compelling evidence in favor of phyletic gradualism. In order to gain insights about the evolution of hydrozoan life history traits, we inferred phylogenetic relationships of 142 species of Thecata (= Leptothecata, Leptomedusae), the most species-rich hydrozoan group, using 3 different ribosomal RNA markers (16S, 18S, and 28S). In conflict with morphology-derived classifications, most thecate species fell in 2 well-supported clades named here Statocysta and Macrocolonia. We inferred many independent medusa losses among Statocysta. Several instances of secondary regain of medusoids (but not of full medusa) from medusa-less ancestors were supported among Macrocolonia. Furthermore, life cycle character changes were significantly correlated with changes affecting colony shape. For both traits, changes did not reflect graded and progressive loss or gain of complexity. They were concentrated in recent branches, with intermediate character states being relatively short lived at a large evolutionary scale. This punctuational pattern supports the existence of 2 alternative stable evolutionary strategies: simple stolonal colonies with medusae (the ancestral strategy, seen in most Statocysta species) versus large complex colonies with fixed gonophores (the derived strategy, seen in most Macrocolonia species). Hypotheses of species selection are proposed to explain the apparent long-term stability of these life history traits despite a high frequency of character change. Notably, maintenance of the medusa across geological time in Statocysta might be due to higher extinction rates for species that have lost this dispersive stage.
Keywords: Cnidaria; colony; Dollo's law; gradualism; Hydrozoa; Leptomedusae; Leptothecata; life cycle; phylogeny; punctuated evolution; reverse evolution; Thecata
Received August 23, 2008; Revised November 13, 2008; Accepted June 30, 2009