An integrative systematic framework helps to reconstruct skeletal evolution of glass sponges (Porifera, Hexactinellida).
BACKGROUND
Glass sponges (Class Hexactinellida) are important components of deep-sea ecosystems and are of interest from geological and materials science perspectives. The reconstruction of their phylogeny with molecular data has only recently begun and shows a better agreement with morphology-based systematics than is typical for other sponge groups, likely because of a greater number of informative morphological characters. However, inconsistencies remain that have far-reaching implications for hypotheses about the evolution of their major skeletal construction types (body plans). Furthermore, less than half of all described extant genera have been sampled for molecular systematics, and several taxa important for understanding skeletal evolution are still missing. Increased taxon sampling for molecular phylogenetics of this group is therefore urgently needed. However, due to their remote habitat and often poorly preserved museum material, sequencing all 126 currently recognized extant genera will be difficult to achieve. Utilizing morphological data to incorporate unsequenced taxa into an integrative systematics framework therefore holds great promise, but it is unclear which methodological approach best suits this task.


RESULTS
Here, we increase the taxon sampling of four previously established molecular markers (18S, 28S, and 16S ribosomal DNA, as well as cytochrome oxidase subunit I) by 12 genera, for the first time including representatives of the order Aulocalycoida and the type genus of Dactylocalycidae, taxa that are key to understanding hexactinellid body plan evolution. Phylogenetic analyses suggest that Aulocalycoida is diphyletic and provide further support for the paraphyly of order Hexactinosida; hence these orders are abolished from the Linnean classification. We further assembled morphological character matrices to integrate so far unsequenced genera into phylogenetic analyses in maximum parsimony (MP), maximum likelihood (ML), Bayesian, and morphology-based binning frameworks. We find that of these four approaches, total-evidence analysis using MP gave the most plausible results concerning congruence with existing phylogenetic and taxonomic hypotheses, whereas the other methods, especially ML and binning, performed more poorly. We use our total-evidence phylogeny of all extant glass sponge genera for ancestral state reconstruction of morphological characters in MP and ML frameworks, gaining new insights into the evolution of major hexactinellid body plans and other characters such as different spicule types.


CONCLUSIONS
Our study demonstrates how a comprehensive, albeit in some parts provisional, phylogeny of a larger taxon can be achieved with an integrative approach utilizing molecular and morphological data, and how this can be used as a basis for understanding phenotypic evolution. The datasets and associated trees presented here are intended as a resource and starting point for future work on glass sponge evolution.
Department of Earth & Environmental Sciences, Palaeontology & Geobiology, Molecular Geo- & Palaeobiology Lab, Ludwig-Maximilians-University Munich, Richard-Wagner-Str. 10, 80333 Munich, Germany.
Martin
M
Dohrmann
Hawaii Undersea Research Laboratory, University of Hawaii at Manoa, 1000 Pope Rd, MSB 229, Honolulu, 96822 HI USA.
Christopher
C
Kelley
Coasts and Oceans National Centre, National Institute of Water and Atmospheric Research (NIWA) Ltd, Private Bag 99940, Newmarket, Auckland, 1149 New Zealand.
Michelle
M
Kelly
Institute of Paleobiology, Polish Academy of Sciences, ul. Twarda 51/55, 00-818 Warszawa, Poland.
Andrzej
A
Pisera
Biodiversity & Geosciences Program, Queensland Museum, South Brisbane, QLD 4101 Australia.|Eskitis Institute for Drug Discovery, Griffith University, Nathan, QLD 4111 Australia.
John N A
JNA
Hooper
Natural History Section, Royal British Columbia Museum, 675 Belleville Street, Victoria, BC V8W 9W2 Canada.|Department of Biology, University of Victoria, 3800 Finnerty Road, Victoria, BC V8P 4H9 Canada.
Henry M
HM
Reiswig
Ancestral state reconstruction; Character evolution; Classification; Hexactinellida; Integrative systematics; Phylogeny; Porifera; Total evidence