Molecular paleobiology of lithistid sponges - reconstructing patterns and timing of diversification
Final Report Abstract
Sponges are sessile benthic organisms that play a significant ecological role in all aquatic habitats. Some sponge groups have contributed to reef-building during long periods of earth history. Reconstructing the phylogenetic relationships of demosponges based on morphology is hampered by the paucity of complex informative characters. Likewise, comparatively little is known from the fossil record due to the poor preservation of sponges. Consequently, our understanding of the diversification of demosponges in deep-time is insufficient.’Lithistid’ demosponges, also referred to as "rock sponges", possess a very rigid skeleton of siliceous spicules. They form a polyphyletic sponge group regarded as pivotal among all demosponges as they display the richest and most continuous fossil record in this class, reaching from the Cambrian to Recent. Therefore, ’lithistids sponges present a promising group for investigating demosponge divergence using a molecular paleobiological approach. However, to date, molecular phylogenetic studies including ’lithistids’ are scarce and their phylogenetic affinities to other demosponges as well as their classification is yet not completely understood. This project contributes to a better understanding of the evolution of ’lithistid’ demosponges. It integrates for the first time both molecular, morphological as well as fossil data in a molecular paleobiological framework to answer pivotal questions on the phylogeny, taxonomy and evolution of this paleontologically immensely important demosponge group. We reveal that the order Tetracinellida, which includes lithistid lineages, is a hotspot for mitochondrial group I introns, which may hamper demosponge phylogenetic reconstructions. Analyzing the largest dataset on sponge mitochondrial group I introns (>95 specimens), we demonstrate that introns in sponges aggregate in the most conserved regions of CO1. We also show horizontal and vertical gene transfer, secondary losses and fungal origin of most sponge group I introns. Several lithistid species new to science are described, including from the poorly investigated deep-water fauna of the Galápagos Archipelago and the Tropical Western Atlantic. In particular the genus Vetulina, a lithistid sponge group with close relationship to freshwater sponges, species is analyzed from the Caribbean, Indian Ocean and the Philippines using molecular clock approaches, indicating that Vetulina presents a relict fauna with its origin in the Tethys Sea. We reconstructed the first dated phylogeny based on complete mitochondrial genomes of Demospongiae. The rich and continuous fossil record of ’lithistids’ were used for calibration and the fossilized birth-death clock model was applied. Results support a Neoproterozoic origin of Demospongiae, a divergence time estimation for the split of freshwater and marine sponges in the Carboniferous, and the possible divergence times of Tetractinellidae (∼315 Ma), the Astrophorina (∼240 Ma), the Spirophorina (∼120 Ma) and the family Corallistidae (∼188 Ma). Discrepancies of our dated phylogeny with their putative first fossil appearance dates were observed and discussed for each sponge group. We provide the currently largest molecular (249 specimens) and morphological (71 specimens) dataset on Tropical Western Atlantic ’lithistid’ demosponges revealing novel insights into the phylogenetic relationships of ’listhistids’, suggesting the revision of the higher-taxa relationships. Several new species, one new genus and one new suborder are proposed. On this groundwork the phylogenetic diversity and bathymetric distribution were analysed, demonstrating that Theonellidae and Corallistidae dominate the fauna, while Neopeltidae and Macandrewiidae are comparatively rare. Additionally, Theonellidae are more abundant in depths <300 m, while Corallistidae dominates deeper habitats >300 m.
Publications
- (2016) A new species of lithistid sponge hiding within the Isabella mirabilis species complex (Porifera: Demospongiae: Tetractinellida) from seamounts of the Norfolk Ridge. Zootaxa 4136: 433-460
Ekins M, Erpenbeck D, Wörheide G, Hooper JNA
(See online at https://doi.org/10.11646/zootaxa.4136.3.2) - (2016). Staying well connected – Lithistid sponges on seamounts. Journal of the Marine Biological Society of the United Kingdom 96 (2): 437-45
Ekins M, Erpenbeck D, Wörheide G, Hooper JNA
(See online at https://doi.org/10.1017/S0025315415000831) - (2017) Dating early animal evolution using phylogenomic data. Scientific Reports 7, 503
Dohrmann M, Wörheide G.
(See online at https://doi.org/10.1038/s41598-017-03791-w) - (2017) Molecular Paleobiology of ’Lithistid’ Demosponges. PhD Thesis, Ludwig-Maximilians-Universität München. 383pp.
Schuster A.
- (2017). Evolution of group I introns in Porifera: new evidence for intron mobility and implications for DNA barcoding. BMC Evolutionary Biology 17(82): 1-21
Schuster A, Lopez JV, Becking LE, Kelly M, Pomponi SA, Wörheide G, Erpenbeck D, Cárdenas P
(See online at https://doi.org/10.1186/s12862-017-0928-9) - (2017). First record of the genus Vetulina Schmidt, 1879 (Porifera: Demospongiae: Sphaerocladina) from the Indian Ocean with the description of two new species: biogeographic and evolutionary significance. Marine Biodiversity
Pisera A, Lukowiak M, Fromont J, Schuster A
(See online at https://doi.org/10.1007/s12526-017-0658-7) - (2018). New species and a molecular dating analysis of Vetulina Schmidt, 1879 (Porifera: Demospongiae: Sphaerocladina) reveal an ancient relict fauna with Tethys origin. Zoological Journal of the Linnean Society
Schuster A, Pisera A, Kelly M, Bell LB, Pomponi SA, Wörheide G, Erpenbeck D
(See online at https://doi.org/10.1093/zoolinnean/zlx114) - (2018). Seven new deep-water Tetractinellida (Porifera: Demospongiae) from the Galá́ pagos Islands – Morphological descriptions and DNA barcodes. Zoological Journal of the Linnean Society
Schuster A, Cárdenas P, Pisera A, Pomponi SA, Kelly M, Wörheide G, Erpenbeck D
