Systematics of 'lithistid' tetractinellid demosponges from the Tropical Western Atlantic-implications for phylodiversity and bathymetric distribution

Abstract

Background: Among all present demosponges, lithistids represent a polyphyletic group with exceptionally well-preserved fossils dating back to the Cambrian. Knowledge of their recent diversity, particularly in the Tropical Western Atlantic Ocean (TWA) where they are common in deep waters, is scarce making any comparison between present and past major 'lithistid' faunas difficult. In addition, the lack of sufficient molecular and morphological data hamper any predictions on phylogenetic relationships or phylodiversity from this region. The Harbor Branch Oceanographic Institute (HBOI, Fort Pierce, Florida) holds the largest collection of TWA lithistid sponges worldwide, however, the majority remain to be taxonomically identified and revised.

Principal findings: In this study we provide sequences of 249 lithistid demosponges using two independent molecular markers (28S rDNA (C1-D2) and cox1 mtDNA). In addition, a morphological documentation of 70 lithistid specimens is provided in the database of the Sponge Barcoding Project (SBP). This integrated dataset represents the largest and most comprehensive of the TWA lithistids to date. The phylogenetic diversity of 'lithistid' demosponges in the Bahamas and Jamaica are high in comparison to other TWA regions; Theonellidae and Corallistidae dominate the fauna, while Neopeltidae and Macandrewiidae are rare. A proposed tetractinellid suborder, one undescribed genus and several undescribed species are recognized and the Pacific 'lithistid' genera, Herengeria and Awhiowhio, are reported from the TWA for the first time. The higher-taxa relationships of desma-bearing tetractinellids are discussed and topics for revision suggested.

Conclusion: This first integrative approach of TWA 'lithistid' demosponges contributes to a better understanding of their phylogenetic affinities, diversity and bathymetric distribution patterns within the TWA. As in the Pacific, the TWA 'lithistid' demosponges dominate deep-water habitats. Deeper taxonomic investigations will undoubtedly contribute to a better comparison between present major 'lithistid' faunas and their fossil record in the Mesozoic.

Keywords: Integrative taxonomy; Lithistiddemosponges; Tetractinellida; Tropical Western Atlantic.

Figure 1. Distribution map of investigated HBOI and other desma-bearing tetractinellids and Vetulinidae from the TWA.

Abbreviations correspond to the different locations (GULF, Gulf of Mexico; CUR, Curaçao; BON, Bonaire; StVIN, St. Vincent; MAR, Martinique; GUAD, Guadaloupe; PUE, Puerto Rico; JAM, Jamaica; HON, Honduras; TUR and CAI, Turks and Caicos; BAH, Bahamas; FLO, Florida). Arrows depict main surface currents. Map generated with GeoMapApp 3.6.3 (http://www.geomapapp.org, Ryan et al., 2009).

Figure 2. Schematic summary cladograms obtained from the 28S and cox1 phylogenies indicating the higher-taxa relationships within the order Tetractinellida.

(A) 28S (B) cox1 summary tree with the suborders Astrophorina (red), Spirophorina (orange) and a proposed suborder (blue, green, pink and light gray) including all rhizoclone desma-bearing families and the families Thrombidae and Stupendidae. Stars behind family names indicate their proposed polyphyly. Dashed lines indicate the uncertainties of not supported topologies. (C) Comparison of current and revised classification including the proposed suborder Thoosina from Carballo et al. (2018).

Figure 3. Bayesian Inference phylogeny of Tetractinellida based on 28S (C1-D2).

Posterior probability (PP) values are provided above or below branches. Self-generated sequences are in bold. Numbers behind taxon names are either voucher numbers or GenBank/ENA accession numbers. Three letter code behind voucher numbers corresponds to the different locations (GULF, Gulf of Mexico; CUR, Curaçao; BON, Bonaire; GUAD, Guadaloupe; PUE, Puerto Rico; JAM, Jamaica; HON, Honduras; TUR, Turks & Caicos; BAH, Bahamas; FLO, Florida; GAL, Galápagos). Taxa where the morphology was investigated are indicated with their corresponding SBD#.

Figure 4. 28S phylogeny continued.

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Figure 5. 28S phylogeny continued.

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Figure 6. 28S phylogeny continued.

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Figure 7. 28S phylogeny continued.

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Figure 8. 28S phylogeny continued.

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Figure 9. Bayesian Inference phylogeny of Tetractinellida based on cox1.

Posterior probability (PP) values are provided above or below branches. Self-generated sequences are in bold. Numbers behind taxon names are either voucher numbers or GenBank/ENA accession numbers. Three letter code behind voucher numbers corresponds to the different locations (GULF, Gulf of Mexico; CUR, Curaçao; BON, Bonaire; GUAD, Guadaloupe; PUE, Puerto Rico; JAM, Jamaica; HON, Honduras; TUR, Turks & Caicos; BAH, Bahamas; FLO, Florida; GAL, Galápagos). Taxa where the morphology was investigated are indicated with their corresponding SBD#.

Figure 10. Cox1 phylogeny continued.

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Figure 11. Cox1 phylogeny continued.

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Figure 12. Cox1 phylogeny continued.

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Figure 13. Cox1 phylogeny continued.

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Figure 14. Cox1 phylogeny continued.

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Figure 15. Cox1 phylogeny continued.

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Figure 16. Cox1 phylogeny continued.

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Figure 17. Rarified inclusive phylogenetic diversity (PD_I) curves per marine regions analyzed.

For a better visualization the PD_I for the Bahamas are illustrated separately (B) due to their larger number of samples.

Figure 18. Bathymetric distribution and relative abundance (%) of TWA desma-bearing demosponges based on 234 samples of eight families.

Numbers in each bar represent the number of samples investigated. The following genera for each family were included: Leiodermatium (Azoricidae); Corallistes, Herengeria, Neophrissospongia and Awhiowhio (Corallistidae); Macandrewia (Macandrewiidae); Daedalopelta and Neopelta (Neopeltidae); Aciculites, Amphibleptula, Microscleroderma, Scleritoderma and Setidium (Scleritodermidae); Gastrophanella and Siphonidium (Siphonidiidae); Discodermia, Racodiscula and Theonella (Theonellidae); Vetulina (Vetulinidae). Geomorphological characterizations of depth zones are given below the graph and follows Pomponi et al. (2001) and Reed & Pomponi (1997).