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Contrasting processes drive ophiuroid phylodiversity across shallow and deep seafloors

Nature volume 565, pages 636–639 (2019)Cite this article

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Abstract

Our knowledge of the distribution and evolution of deep-sea life is limited, impeding our ability to identify priority areas for conservation1. Here we analyse large integrated phylogenomic and distributional datasets of seafloor fauna from the sea surface to the abyss and from equator to pole of the Southern Hemisphere for an entire class of invertebrates (Ophiuroidea). We find that latitudinal diversity gradients are assembled through contrasting evolutionary processes for shallow (0–200 m) and deep (>200 m) seas. The shallow-water tropical–temperate realm broadly reflects a tropical diversification-driven process that shows exchange of lineages in both directions. Diversification rates are reversed for the realm that contains the deep sea and Antarctica; the diversification rates are highest at polar and lowest at tropical latitudes, and net exchange occurs from high to low latitudes. The tropical upper bathyal (200–700 m deep), with its rich ancient phylodiversity, is characterized by relatively low diversification and moderate immigration rates. Conversely, the young, specialized Antarctic fauna is inferred to be rebounding from regional extinctions that are associated with the rapid cooling of polar waters during the mid-Cenozoic era.

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Fig. 1: Analyses of phylodiversity across the seafloor.
Fig. 2: Biomes possess divergent phylogenetic signatures.
Fig. 3: Distinct pathways of diversification and migration occur in shallow and deep seas.

Data availability

All data necessary to repeat the analyses described here have been made available through the Dryad digital data repository (https://doi.org/10.5061/dryad.9jk90f6).

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Acknowledgements

T.D.O., A.F.H. and N.J.B. were supported by the Marine Biodiversity Hub, funded through the National Environmental Science Program (NESP) and administered through the Australian Government’s Department of the Environment and Energy. S.N.C.W. was supported by the Global Ocean Biodiversity Initiative funded by the International Climate Initiative (IKI). CSIRO Marine National Facility provided sea time and personnel on the RV Investigator for the ‘Sampling the abyss’ voyage IN2017_V03. Museums Victoria and Muséum National d’Histoire Naturelle, Paris provided the majority of tissue samples. K. Naughton extracted the DNA; library preparation, target capture and sequencing was done through the Georgia Genomics Facility and Arbor Biosciences.

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Nature thanks D. Allen, F. L. Condamine, P. Snelgrove and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Authors and Affiliations

  1. Museums Victoria, Melbourne, Victoria, Australia

    Timothy D. O’Hara, Andrew F. Hugall, Skipton N. C. Woolley & Guadalupe Bribiesca-Contreras

  2. CSIRO Oceans and Atmosphere, Hobart, Tasmania, Australia

    Skipton N. C. Woolley & Nicholas J. Bax

  3. Biosciences, University of Melbourne, Melbourne, Victoria, Australia

    Guadalupe Bribiesca-Contreras

  4. Institute for Marine and Antarctic Science, University of Tasmania, Hobart, Tasmania, Australia

    Nicholas J. Bax

Authors
  1. Timothy D. O’Hara
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Contributions

T.D.O. and A.F.H. designed the research and assembled the data. T.D.O., A.F.H. and S.N.C.W. performed the phylodiversity analyses and T.D.O., A.F.H. and G.B.-C. performed the macro-evolutionary analyses. All authors contributed to interpretation and discussion of results. T.D.O., A.F.H. and N.J.B. drafted the paper with substantial input from all authors.

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Correspondence to Timothy D. O’Hara.

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Extended data figures and tables

Extended Data Fig. 1 Maps and plots of collection and sequencing effort.

a, Map of sample sites across the study area, with land masses defined using the ETOPO1 dataset62. The study area, a trapezoid shape on this geographical projection, contains equal area polygons per latitude spaced either side of 150° E. Red dots indicate shallow sites (0–200 m), green dots indicate samples obtained from the upper to mid-bathyal (200–2,000 m) and blue dots indicate samples from the lower bathyal and abyss (>2,000 m); many sites overlap. Sampling over our study area is concentrated around continental margins with few expeditions to the abyssal plain or mid-ocean ridges. b, Collection effort (for example, the numbers of trawls, dredges or submersible collections) over our study area is, as expected, highest in shallow water (0–100 m) followed by cells at upper to mid-bathyal depths. Variation in collection effort does not explain the latitudinal and bathymetric gradients in species richness for this data8. Although collection effort is much lower at lower bathyal and abyssal depths (2,000–4,000 m), this is offset by a general increase in the size of observed species ranges with depth. Many abyssal ophiuroids are widespread across temperate and tropical latitudes. c, The percentage of species with DNA data is high (>70%) over the entire study area, except below 2,000 m across tropical latitudes (mean, 52%; minimum, 41%). However, these depths are relatively species-poor and sequencing effort across the entire tropical deep-sea biome (as defined in Fig. 1g) exceeds 70%.

Extended Data Fig. 2 Latitudinal and bathymetric gradients for species richness, family richness and phylogenetic diversity.

a–f, Latitudinal (a, c, e) and bathymetric (b, d, f) gradients are shown for species richness (a, b), family richness (c, d) and phylogenetic diversity (e, f). Diversity peaks between 13 and 23° S and at a depth of between 200 and 700 m, declining in polar regions and abyss. A sub-equatorial peak of richness for shallow marine fauna has been observed for many marine datasets63. Across all latitudes, the bathymetric peak is in the upper to mid-bathyal, a pattern also recorded for numerous other eurybathyal invertebrates12,13,14. Our temperate mid-bathyal (1,000 m) latitudinal peak is compatible with northern Atlantic Ocean studies7. A, end of the Australian continental shelf; N, end of the New Zealand continental shelf; P, temperate–polar transition (south of Macquarie Island); T, tropical–temperate transition.

Extended Data Fig. 3 Additional latitudinal and bathymetric plots of diversity indices.

a, High levels of family-level richness extend into temperate regions and mid-bathyal depths. b, Phylogenetic radiations are concentrated in upper tropical habitats and Antarctica. c, The pattern of normalized mean phylogenetic pairwise distance between cells is similar to relative phylogenetic diversity (Fig. 1c). d, The frequency that observed phylogenetic diversity exceeded null models (in which randomized species are present in each cell while retaining cell species richness). e, f, Simpson’s phylogenetic beta diversity (Fig. 1f) factored into latitudinal (e) and bathymetric (f) components.

Extended Data Fig. 4 MuSSE randomization trials.

a–c, Comparison of speciation (a), extinction (b) and transition (c) rates generated from our MuSSE Bayesian MCMC analysis (n = 10,000) compared to maximum likelihood analyses that resampled (n = 400) states (biomes) within species with multi-biome distributions. Box plots show the median, upper and lower quartile (boxes), and minimum and maximum (whiskers) rate values. The resampling results (blue) are broadly similar to the original MCMC run (green), indicating that biome misclassification did not significantly affect the results. One exception is the temperate shallow (TempS) to tropical shallow (TropS) transition rates, which were significantly different for resampling owing to the occurrence of subtropical species across the transition zone.

Extended Data Fig. 5 Phylodiversity and rate plots of ophiuroid subclades.

a–c, The three major clades of extant Ophiuroidea10,36 contribute differently to overall patterns of phylogenetic diversity across our five biomes (Fig. 2). a, Clade A is rich in deep-sea and Antarctic species, although individual families have divergent distributions. The Antarctic is dominated by the Ophiopyrgidae whereas the Ophiomusaidae, Ophiosphalmidae, Astrophytidae and Euryalidae are largely absent from this region. Clade A has low species richness in the two shallow-water biomes. b, Clade B is rich in the tropical shallow, tropical deep-sea and temperate deep-sea biomes. It consists of one suborder (Ophiodermatina) that is heavily represented in tropical shallow-water biome and another (Ophiacanthina) that is largely present in deep-sea habitats, particularly on hard substrata such as seamounts. c, Clade C on the other hand is rich in tropical and temperate shallow-water biomes, including the families Ophiolepididae, Ophionereididae, Amphiuridae and Ophiotrichidae, and has relatively few lineages in the deep sea or Antarctica. d, Antarctic biome diversification rates are increased compared to other biomes. e, f, However, this is not an artefact of lowered molecular substitution rates or dominance by the family Ophiopyrgidae, as demonstrated by histograms of DR statistic rates (e) and PLRS estimated tip substitution rates (f), averaged by species per family per biome. Families per biomes with fewer than three species were omitted; Ophiopyrgidae are highlighted by stripes. Antarctic species in multiple families do not have relatively low molecular rates. Using the root-to-tip path length of the RAxML tree instead of substitution rate essentially gives the same result. Even within the Ophiopyrgidae, diversification rates for Antarctic species are much higher than for non-Antarctic species.

Extended Data Fig. 6 Environmental patterns.

a–d, Mean annual environmental data for each latitudinal (1.0°) and bathymetric (100 m) cell across our study area for comparison with phylodiversity analyses. A lens of relatively hot (a) salty (b) water occurs at shallow depths across tropical and temperate latitudes (0–40° S). Antarctic intermediate water sinks at sub-Antarctic latitudes and flows north to subtropical latitudes (20° S) at mid-bathyal depths (around 1,000 m). c, Deoxygenated ‘deep’ water flows southwards from the northern hemisphere at lower bathyal depths, shoaling off the Antarctic continent. Cold, dense, oxygen-rich ‘bottom’ water sinks near Antarctica, flowing northwards at abyssal depths. d, Yearly net primary production peaks at temperate latitudes over the study area, driving elevated carbon flux to the seafloor; Antarctic production is highly seasonal. e, Area of depth strata per degree of latitude across the study region, calculated by counting the number of cells of each category for each degree of latitude in the ETOPO162 raster GIS layer (0.01° resolution) and adjusting for the reducing circumference of the Earth with increased latitude. There is limited terrestrial, sublittoral and upper bathyal habitat in the Southern Ocean between the Australian/New Zealand continental masses and Antarctica.

Extended Data Fig. 7 Beta diversity and phylogenetic beta diversity.

Ordinations (nMDS), cluster dendrograms (UPGMA) and latitudinal and bathymetric representations of (phylogenetic) beta diversity clusters for each 1.0° latitude × 100 m depth cell across our study region. a–c, Simpson’s phylogenetic beta diversity (pβSim) (a), Sorensen’s phylogenetic beta diversity (pβSor) (b) and Simpson’s beta diversity of the presence–absence of species (βSim) (c). Nine clusters (vertical red lines) are coloured to highlight coherent patterns across latitude and depth. The three methods showed broad similarities in grouping the fauna into tropical, temperate and polar regions and sublittoral, upper bathyal and lower bathyal–abyssal depth strata, although the cluster hierarchy can differ. The pβSim and βSim plots emphasized the strong compositional turnover between 100 and 300 m at tropical and temperate latitudes (Fig. 1f and Extended Data Fig. 3e). pβSor—which emphasizes species richness gradients in addition to compositional turnover—clustered upper to mid-bathyal cells (200–2,000 m) separately from those in the lower bathyal and abyss (>2,000 m), reflecting a zone of higher species richness and relative phylogenetic diversity (Fig. 1). The pβSim and βSim analyses also identified a small shallow-water subtropical cluster that reflects the heightened latitudinal turnover between 30 and 40° S9. The pβSor analysis separated two species-poor Antarctic deep-sea regions. The extent of the temperate sublittoral zone varied among analyses, possibly owing to it being a small zone of admixture and turnover. The number of clusters was reduced to five (Fig. 1g) for the MuSSE analyses (see Methods for rationale).

Extended Data Table 1 Biome parameter estimates
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Extended Data Table 2 One-sided significance tests of the hypotheses
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O’Hara, T.D., Hugall, A.F., Woolley, S.N.C. et al. Contrasting processes drive ophiuroid phylodiversity across shallow and deep seafloors. Nature 565, 636–639 (2019). https://doi.org/10.1038/s41586-019-0886-z

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