Evolution in the North American Basin

In the 1990s, we began a NSF supported program of research to measure population genetic structure in deep-sea mollusks. This was the first concerted effort to study the genetic basis of population differentiation in the deep sea, apart from hydrothermal vents.  A major breakthrough was our development of molecular genetic techniques to work with formalin-fixed small (<1mm) invertebrates.  These new genetic methods made it possible to use extensive available collections of deep-sea species to explore the evolutionary-historical basis of deep-sea biodiversity on global scales, and added a new dimension to the use of museum collections in general for spatial and temporal analyses of population structure.

Using these techniques, we quantified the population genetic structure of several molluscan species arrayed along a depth gradient in the western North Atlantic (see Fig.1). Genetic divergence among populations decreased with depth suggesting that the potential for population differentiation and speciation varied bathymetrically (Fig. 2).  Patterns of genetic variation also indicated that deep-sea macrofauna could have strong population structure over small spatial scales (Fig. 3), similar to shallow-water and terrestrial organisms.  Genetic divergence was sufficiently large for some species that they may represent cryptic species complexes (Fig. 4).  We also quantified the genetic structure of several protobranch bivalves and gastropods at ocean-wide scales to test hypotheses about how major current and topographic features limit gene flow (Fig.s 5-7).  Patterns of genetic variation differed for bathyal and abysssal species suggesting they are influenced differently by deep-water currents and the Mid-Atlantic Ridge. Our research is providing the genetic tools to explore population structure in the deep sea, and producing the first critical evidence of how and where evolutionary differentiation occurs in this vast and complex ecosystem.  Below is a description of our ongoing research programs and questions.

1) Depth-Differentiation Hypothesis

The deep sea is now known to be highly complex with strong geographic and bathymetric gradients that might influence the location, scales and dynamics of evolution.  The rate of environmental change is a function of the rate of change in depth and proximity to coastal production. In the more steeply descending bathyal zone, depth parallels gradients of decreasing temperature, decreasing metabolic rates and increasing pressure. The bathyal zone is also a heterogeneous environment on large and small spatial scales. Not surprisingly, with strong vertical environmental gradients and a fragmented heterogeneous landscape, the bathyal zone supports high alpha and beta species diversity. The strong environmental gradients and greater biotic and abiotic heterogeneity at bathyal depths might impose different selective regimes that increase the probability of population differentiation and speciation.

Because of its close proximity to land and coastal systems, the bathyal zone must have been strongly impacted by global climatic and oceanographic changes in the past.  Variation in surface production caused by glacial cycles must have caused strong population fluctuations and bathymetric range displacement. The combination of paleoenvironmental change, fluctuations in populations size and the isolating effects of slope erosion during glaciation might have promoted population differentiation in the bathyal zone by both selective and non-selective mechanisms. The deeper, more remote, more uniform and topographically simpler environment of the abyssal plain is probably considerably less conducive to evolutionary divergence.

In addition to the more pronounced spatial and temporal environmental heterogeneity at bathyal depths, several lines of evidence support the notion that this region promotes population differentiation and speciation.  First, intraspecific population genetic divergence is greater at bathyal than abyssal depths for both mollusks and crustaceans. Second, phenotypic divergence as measured by multivariate morphological change in shell architecture in gastropods decreases exponentially with depth paralleling bathymetric patterns in genetic divergence.  Third, recent evidence from paleontology, comparative phylogenetics, and molecular evolution suggest that geographic variation in evolutionary rates may play an important role in producing large-scale gradients in diversity.  Similarly, depth-related variation in evolutionary rates might help explain why species diversity is greatest at bathyal depths. 

The intraspecific patterns of genetic variation within and among species, the morphological divergence and the correlation between evolutionary rates and species diversity all suggest the bathyal region may be an evolutionary hot spot for the genesis of the endemic deep-sea fauna.  We are testing the hypothesis that population differentiation in deep-sea mollusks decrease with depth.  This involves quantifying geographic and bathymetric patterns of variation in both nuclear and mitochondrial genes for a series of clams and snails along a depth gradient (500-5000m) in the western north Atlantic.

2) Forces Creating a Genetic Break at 3300m

Our previous research revealed a pronounced genetic separation between populations of the protobranch bivalve Deminucula atacellana above and below 3300 m.  Populations on either side of 3300 m possess highly divergent haplotypes (Fig. 2).  The strong population divergence was unexpected and perplexing because there are no obvious oceanographic or topographic features that would limit gene flow between these regions.  A similar break at 3300 m has been found for D. atacellana in the South Atlantic, although the data are more limited.

Interestingly, D. atacellana is not the only species to show a sharp break at 3300 m.  In a global analysis of population structure in the cosmopolitan amphipod Eurythenes gryllus , France and Kocher (1996) found a similar pattern at virtually the same depth (Fig. 9).  At abyssal depths, Atlantic and Pacific populations of E. gryllus were genetically homogeneous, but in both oceans, there was a pronounced divergence (16 S mtDNA) among populations above and below 3200m. The bathymetric divergence within ocean basins far exceeded that found between the Atlantic and Pacific populations at similar depths. These two species have extremely different life styles, natural histories, phylogenetic affinities and geographic distributions.  Their congruent genetic divergence at 3300 m in vastly different regions of the world oceans, suggests that 3300m may represent a ubiquitous unrecognized phylogeographic barrier isolating organisms inhabiting different depth regimes. 

In our work we are exploring the forces that might produce such a sharp genetic discontinuity among multiple unrelated species.

3) Testing the Source-Sink Hypothesis of Abyssal Biodiversity

Studies of species diversity have centered almost exclusively on patterns of a–diversity in samples arrayed along a depth gradient.  The principal finding of these studies is that diversity is high in the bathyal zone (200-4000 m) and then decreases markedly in the abyss (> 4000 m).  This decline in diversity coincides with the exponential decrease in benthic standing stock caused by the reduction in carbon flux to the seafloor from overhead production that occurs with increased depth and distance from productive coastal waters.  The simplest explanation for depressed abyssal diversity is that it represents an Allee Effect – densities of many populations become so extraordinarily low that they are no longer reproductively viable.

Rex et al. (2005) compiled comprehensive databases (from regional systematic monographs and biotic surveys) of the bathymetric ranges of gastropods and bivalves in the deep basins of the eastern and western North Atlantic.  When diversity is estimated as the number of coexisting ranges in successive depth intervals, diversity peaks at bathyal depths just as shown by a–diversity trends.  However, the distribution of ranges reveals something that a–diversity cannot.  The abyssal molluscan fauna is primarily an attenuation of the bathyal fauna with little evidence of endemism.  It is made up of deeper range extensions of a subset of bathyal species living at extremely low densities.  For most abyssal populations density seems much too low to permit successful reproduction.  The vast majority of these species have larval dispersal.  These distributional and life-history patterns suggest a new explanation for abyssal biodiversity.  For many species, bathyal and abyssal populations may constitute a source-sink system driven by a steep gradient in nutrient availability in which abyssal populations are regulated by a balance between chronic local extinction from inverse density dependence and immigration from bathyal sources. 

To test the Source-Sink hypothesis we are testing a series of specific predictions about the genetic consequences of source-sink dynamics (e.g. dispersal should be unidirectional, no unique abyssal haplotypes, etc.). The source-sink hypothesis also predicts that rare abyssal populations will show less reproductive maturity and, particularly, mating success than their more abundant bathyal counterparts. In collaboration with Paul Tyler’s lab at Southampton Oceanographic Center, we will histologically section conspecific representatives of bathyal and abyssal populations to test this prediction.

General Sampling Program

To test the hypotheses outlined above, we took 28 epibenthic sled samples along a depth gradient from south of Cape Cod, Massachusetts to Bermuda (Fig. 1).  The samples were taken evenly spaced from 1000-5000m depth along the transect shown in Fig. 1.  We also sampled more intensively between 2500 and 3500m to test hypothesis 2 and at abyssal depths to test hypothesis 3.  The transect parallels the Gay Head- Bermuda transect (GBT) of the Woods Hole Oceanographic sampling program of the 1960s to allow us to ultimately test temporal changes in haplotype frequencies of mtDNA.