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Review
, 89 (2), 406-26

Explaining Bathymetric Diversity Patterns in Marine Benthic Invertebrates and Demersal Fishes: Physiological Contributions to Adaptation of Life at Depth

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Review

Explaining Bathymetric Diversity Patterns in Marine Benthic Invertebrates and Demersal Fishes: Physiological Contributions to Adaptation of Life at Depth

Alastair Brown et al. Biol Rev Camb Philos Soc.

Abstract

Bathymetric biodiversity patterns of marine benthic invertebrates and demersal fishes have been identified in the extant fauna of the deep continental margins. Depth zonation is widespread and evident through a transition between shelf and slope fauna from the shelf break to 1000 m, and a transition between slope and abyssal fauna from 2000 to 3000 m; these transitions are characterised by high species turnover. A unimodal pattern of diversity with depth peaks between 1000 and 3000 m, despite the relatively low area represented by these depths. Zonation is thought to result from the colonisation of the deep sea by shallow-water organisms following multiple mass extinction events throughout the Phanerozoic. The effects of low temperature and high pressure act across hierarchical levels of biological organisation and appear sufficient to limit the distributions of such shallow-water species. Hydrostatic pressures of bathyal depths have consistently been identified experimentally as the maximum tolerated by shallow-water and upper bathyal benthic invertebrates at in situ temperatures, and adaptation appears required for passage to deeper water in both benthic invertebrates and demersal fishes. Together, this suggests that a hyperbaric and thermal physiological bottleneck at bathyal depths contributes to bathymetric zonation. The peak of the unimodal diversity-depth pattern typically occurs at these depths even though the area represented by these depths is relatively low. Although it is recognised that, over long evolutionary time scales, shallow-water diversity patterns are driven by speciation, little consideration has been given to the potential implications for species distribution patterns with depth. Molecular and morphological evidence indicates that cool bathyal waters are the primary site of adaptive radiation in the deep sea, and we hypothesise that bathymetric variation in speciation rates could drive the unimodal diversity-depth pattern over time. Thermal effects on metabolic-rate-dependent mutation and on generation times have been proposed to drive differences in speciation rates, which result in modern latitudinal biodiversity patterns over time. Clearly, this thermal mechanism alone cannot explain bathymetric patterns since temperature generally decreases with depth. We hypothesise that demonstrated physiological effects of high hydrostatic pressure and low temperature at bathyal depths, acting on shallow-water taxa invading the deep sea, may invoke a stress-evolution mechanism by increasing mutagenic activity in germ cells, by inactivating canalisation during embryonic or larval development, by releasing hidden variation or mutagenic activity, or by activating or releasing transposable elements in larvae or adults. In this scenario, increased variation at a physiological bottleneck at bathyal depths results in elevated speciation rate. Adaptation that increases tolerance to high hydrostatic pressure and low temperature allows colonisation of abyssal depths and reduces the stress-evolution response, consequently returning speciation of deeper taxa to the background rate. Over time this mechanism could contribute to the unimodal diversity-depth pattern.

Keywords: colonisation; deep sea; diversity; evolution; hydrostatic pressure; invertebrate; macroecology; radiation; speciation; temperature.

Figures

Fig. 1
Fig. 1
Conceptual profile of a passive aseismic continental margin (Adapted from Gage & Tyler, 1991). Horizontal bars on the left indicate percentage of total ocean surface area of each 100 m depth interval (note that this is not restricted exclusively to continental margins) estimated from figure 9.2 in Mackenzie & Lerman (2006) (black scale bar = 5%; depths greater than 5000 m not shown). In topographic terms, the continental shelf extends to the shelf break where the topographic gradient increases, characterising the continental slope. The topographic gradient reduces onto the continental rise, formed by a thick slope-derived sediment wedge, and reduces further onto the relatively flat abyssal plain. The continental margin comprises continental shelf, slope and rise; the deep continental margin comprises continental slope and rise. Ecological zones are bathyal (200–4000 m) and abyssal (4000–6000 m). Conceptual components of bathymetric patterns of diversity (Adapted from Carney, ; height = bathymetric range, width = species richness) are included, representing three groups of species: upper boundary biota (UBB) species extend downwards from or above the upper boundary of the deep continental margin but do not reach the lower boundary; lower boundary biota (LBB) species extend upwards from or below the lower boundary of the deep continental margin but do not reach the upper boundary; inter-boundary biota (IBB) species reach neither boundary. Shaded areas indicate depths of high species turnover consistently identified in studies of bathymetric diversity (Carney, 2005). A unimodal diversity–depth pattern typically peaks between 1000 and 3000 m despite the relatively low area represented by these depths.
Fig. 2
Fig. 2
Experimentally determined hydrostatic pressure tolerances (white bars) and reported adult bathymetric distributions of shallow-water benthic invertebrate species (black bars). Tolerances presented are for the most developmentally advanced stage examined at ecologically relevant temperatures and are determined by a variety of measures (see Table 2 for details). Studies using coarse measures or temperatures not ecologically relevant are excluded. Asterisks indicate tolerance of the highest hydrostatic pressure assessed. °, Note that the slight discrepancy in hydrostatic pressure tolerance and adult bathymetric distribution of Anonyx nugax is likely to result from the resolution of pressure treatments used to assess hydrostatic pressure tolerance. Maximum tolerance is consistently identified at bathyal pressures, indicating that temperature and pressure equating to these depths may impose a physiological bottleneck at bathyal depths on shallow-water fauna colonising the deep sea following mass extinctions. This coincides with high bathymetric turnover of species, suggesting that the hyperbaric and thermal physiological bottleneck contributes to bathymetric zonation.
Fig. 3
Fig. 3
Scenario for colonisation of the deep sea following dysoxic mass extinction. An enduring upper boundary biota (UBB) species extends its distribution downslope to a taxon-specific maximum depth at the physiological bottleneck determined by interacting effects of high hydrostatic pressure and low temperature (solid line). At this limit hyperbaric and thermal stress increases mutation in germ cells, inactivates canalisation during embryonic or larval development, releases hidden genetic variation or increases mutagenic activity, or activates or releases transposable elements in larval or adult organisms, increasing genetic or phenotypic variation. Greater variation unrelated to hydrostatic pressure or temperature tolerance results in significantly increased parapatric or sympatric speciation of UBB species or inter-boundary biota (IBB) species into niches left vacant by mass extinction (dotted lines). These remain bathymetrically constrained by the combined effects of high hydrostatic pressure and low temperature. Species remain under stress promoting continuing elevated variation, and speciation rate remains increased. Variation increasing tolerance of high hydrostatic pressure or low temperature instead results in parapatric or peripatric speciation of lower boundary (LBB) species (dashed lines). Increased tolerance of high hydrostatic pressure or low temperature diminishes the stress effect and returns variation to background rate. The differential rates of speciation over time result in the unimodal pattern of biodiversity with depth. Experimental evidence indicates consistently that critical pressure and temperature conditions for shallow-water benthic invertebrate species equate to the bathyal environment, and the unimodal diversity–depth pattern typically peaks at these depths.

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