Ron J. Etter

A Source-Sink Hypothesis for Abyssal Biodiversity

Bathymetric gradients of biodiversity in the deep‐sea benthos constitute a major class of large‐scale biogeographic phenomena. They are typically portrayed and interpreted as variation in α diversity (the number of species recovered in individual samples) along depth transects. Here, we examine the depth ranges of deep‐sea gastropods and bivalves in the eastern and western North Atlantic. This approach shows that the abyssal molluscan fauna largely represents deeper range extensions for a subset of bathyal species. Most abyssal species have larval dispersal, and adults live at densities that appear to be too low for successful reproduction. These patterns suggest a new explanation for abyssal biodiversity. For many species, bathyal and abyssal populations may form a source‐sink system in which abyssal populations are regulated by a balance between chronic extinction arising from vulnerabilities to Allee effects and immigration from bathyal sources. An increased significance of source‐sink dynamics with depth may be driven by the exponential decrease in organic carbon flux to the benthos with increasing depth and distance from productive coastal systems. The abyss, which is the largest marine benthic environment, may afford more limited ecological and evolutionary opportunity than the bathyal zone.

POPULATION DIFFERENTIATION DECREASES WITH DEPTH IN DEEP-SEA BIVALVES

Abstract The deep sea is the largest ecosystem on Earth. Recent exploration has revealed that it supports a highly diverse and endemic benthic invertebrate fauna, yet the evolutionary processes that generate this remarkable species richness are virtually unknown. Environmental heterogeneity, topographic complexity, and morphological divergence all tend to decrease with depth, suggesting that the potential for population differentiation may decrease with depth.To test this hypothesis, we use mitochondrial DNA (16S rRNA gene) to examine patterns of population differentiationin four species of protobranch bivalves (Nuculoma similis, Deminucula atacellana, Malletia abyssorum, and Ledellaultima) distributed along a depth gradient in the western North Atlantic. We sequenced 268 individuals from formalinfixed samples and found 45 haplotypes. The level of sequence divergence among haplotypes within species was similar, but shifted from between populations at bathyal depths to within populations at abyssal depths. Levels of population structure as measured by ST were considerably greater in the upper bathyal species (N. similis= 0.755 and D. atacellana= 0.931; 530–3834 m) than in the lower bathyal/abyssal species (M. abyssorum= 0.071 and L. ultima= 0.045; 2864–4970 m). Pairwise genetic distances among the samples within each species also decreased with depth. Population trees (UPGMA) based on modified coancestry coefficients and nested clade analysis both indicated strong population‐level divergence in the two upper bathyal species but little for the deeper species. The population genetic structure in these protobranch bivalves parallels depth‐related morphological divergence observed in deep‐sea gastropods.The higher level of genetic and morphological divergence, coupled with the strong biotic and abiotic heterogeneityal bathyal depths, suggests this region may be an active area of species formation. We suggest that the steep, topographically complex, and dynamic bathyal zone, which stretches as a narrow band along continental margins, plays a more important role in the evolutionary radiation of the deep‐sea fauna than the much more extensive abyss.

Bathymetric patterns of body size: implications for deep-sea biodiversity

Abstract The evolution of body size is a problem of fundamental interest, and one that has an important bearing on community structure and conservation of biodiversity. The most obvious and pervasive characteristic of the deep-sea benthos is the small size of most species. The numerous attempts to document and explain geographic patterns of body size in the deep-sea benthos have focused on variation among species or whole faunal components, and have led to conflicting and contradictory results. It is important to recognize that studying size as an adaptation to the deep-sea environment should include analyses within species using measures of size that are standardized to common growth stages. An analysis within eight species of deep-sea benthic gastropods presented here reveals a clear trend for size to increase with depth in both larval and adult shells. An ANCOVA with multiple comparison tests showed that, in general, size–depth relationships for both adult and larval shells are more pronounced in the bathyal region than in the abyss. This result reinforces the notion that steepness of the bathymetric selective gradient decreases with depth, and that the bathyal region is an evolutionary hotspot that promotes diversification. Bathymetric size clines in gastropods support neither the predictions of optimality models nor earlier arguments based on tradeoffs among scaling factors. As in other environments, body size is inversely related to both abundance and species density. We suggest that the decrease in nutrient input with depth may select for larger size because of its metabolic or competitive advantages, and that larger size plays a role in limiting diversity. Adaptation is an important evolutionary driving force of biological diversity, and geographic patterns of body size could help unify ecological and historical theories of deep-sea biodiversity.

Bathymetric and geographic population structure in the pan‐Atlantic deep‐sea bivalve Deminucula atacellana (Schenck, 1939)

The deep‐sea soft‐sediment environment hosts a diverse and highly endemic fauna of uncertain origin. We know little about how this fauna evolved because geographic patterns of genetic variation, the essential information for inferring patterns of population differentiation and speciation are poorly understood. Using formalin‐fixed specimens from archival collections, we quantify patterns of genetic variation in the protobranch bivalve Deminucula atacellana, a species widespread throughout the Atlantic Ocean at bathyal and abyssal depths. Samples were taken from 18 localities in the North American, West European and Argentine basins. A hypervariable region of mitochondrial 16S rDNA was amplified by polymerase chain reaction (PCR) and sequenced from 130 individuals revealing 21 haplotypes. Except for several important exceptions, haplotypes are unique to each basin. Overall gene diversity is high (h = 0.73) with pronounced population structure (ΦST = 0.877) and highly significant geographic associations (P < 0.0001). Sequences cluster into four major clades corresponding to differences in geography and depth. Genetic divergence was much greater among populations at different depths within the same basin, than among those at similar depths but separated by thousands of kilometres. Isolation by distance probably explains much of the interbasin variation. Depth‐related divergence may reflect historical patterns of colonization or strong environmental selective gradients. Broadly distributed deep‐sea organisms can possess highly genetically divergent populations, despite the lack of any morphological divergence.

PHYSIOLOGICAL STRESS AND COLOR POLYMORPHISM IN THE INTERTIDAL SNAIL NUCELLA LAPILLUS

The intertidal snail Nucella lapillus exhibits considerable variation in shell color both within and between populations differentially exposed to wave action. Populations from high‐wave‐energy shores tended to be highly polymorphic and were dominated by pigmented morphs (especially brown), while those at more sheltered locations exhibited less polymorphism and were predominantly white. Field and laboratory experiments were conducted to determine the role of physiological stress and selective predation in maintaining the observed distribution of color morphs.

Integrating genetic and environmental forces that shape the evolution of geographic variation in a marine snail

Temporal and spatial patterns of phenotypic variation have traditionally been thought to reflect genetic differentiation produced by natural selection. Recently, however, there has been growing interest in how natural selection may shape the genetics of phenotypic plasticity to produce patterns of geographic variation and phenotypic evolution. Because the covariance between genetic and environmental influences can modulate the expression of phenotypic variation, a complete understanding of geographic variation requires determining whether these influences covary in the same (cogradient variation) or in opposing (countergradient variation) directions. We focus on marine snails from rocky intertidal shores as an ideal system to explore how genetic and plastic influences contribute to geographic and historical patterns of phenotypic variation. Phenotypic plasticity in response to predator cues, wave action, and water temperature appear to exert a strong influence on small and large-scale morphological variation in marine snails. In particular, plasticity in snail shell thickness: (i) may contribute to phenotypic evolution, (ii) appears to have evolved across small and large spatial scales, and (iii) may be driven by life history trade-offs tied to architectural constraints imposed by the shell. The plasticity exhibited by these snails represents an important adaptive strategy to the pronounced heterogeneity of the intertidal zone and undoubtedly has played a key role in their evolution.

Asymmetrical developmental plasticity in an intertidal snail

Field and laboratory experiments were used to investigate the variation and phenotypic plasticity in the adhesive abilities of the intertidal snail Nucella lapillus between high‐ and low‐wave‐energy environments. Whelks from an exposed coast produced a larger pedal surface area and were more resistant to dislodgement than were similar‐sized individuals from a protected shore. Tenacity (g/cm2) was similar between individuals from exposed and protected shores, indicating that variation in resisting dislodgement was solely a function of pedal surface area.

A genetic dimension to deep-sea biodiversity

Our knowledge of deep-sea biodiversity is based almost entirely on morphological distinctions at the species level. Here, we use haplotype variations in the mitochondrial 16S ribosomal gene to assess biodiversity at the genome level in four deep-sea molluscan morphospecies. Genetic divergence levels among populations of the morphospecies fall within the range of interspecific divergence found in coastal marine and aquatic molluscan genera. Results indicate a rich population structure at the genetic level in deep-sea mollusks, and suggest the possibility that some seemingly coherent morphospecies are composed of cryptic species.

The effect of wave action, prey type, and foraging time on growth of the predatory snail Nucella lapillus (L.)

Abstract Growth rates of intertidal snails vary among populations differentially exposed to wave action; individuals from sheltered habitats typically grow more quickly than do those from more exposed coasts. A series of field and laboratory experiments were conducted to separate the genetic and phenotypic components of this variation in Nucella lapillus (L.) and to investigate the extent to which prey type and foraging time, which also vary across the wave-exposure gradient, affect growth. Juvenile and adult whelks were reciprocally transplanted between an exposed and a protected shore and subsequent growth followed. Independent of origin, whelks grew more on the sheltered shore. By contrast, growth rates for snails from exposed and protected shores were similar when reared under uniform conditions in the laboratory. Together these findings suggest that the variation observed in nature does not represent genetic differentiation, but reflects the influence of proximal factors that depress growth on wave-swept shores. Growth rates of juveniles from exposed and protected shores maintained in the laboratory on a diet of an overabundance of (1) barnacles, (2) mussels, (3) both, and (4) both, but only 67% of the time, indicated that prey type and foraging time affect growth. Whelks grew best on a diet of mussels, either singly or in combination with barnacles, grew less on barnacles alone, and least when foraging time was restricted. Because growth rates on specific prey in the laboratory were opposite the observed trend in nature, variation in prey across the exposure gradient cannot be invoked to account for the difference in growth between N. lapillus from exposed and protected shores. The slower growth rates when foraging time was restricted are consistent with the notion that wave energies on exposed coasts depress growth by limiting foraging time or by reducing foraging efficiency.

SHADING FACILITATES SESSILE INVERTEBRATE DOMINANCE IN THE ROCKY SUBTIDAL GULF OF MAINE

Dramatic shifts in community composition occur between vertical and horizontal rocky surfaces in subtidal environments worldwide, yet the forces mediating this transition are poorly understood. Vertical rock walls are often covered by lush, diverse communities of sessile suspension-feeding invertebrates, while adjacent horizontal substrates are dominated by algae, or corals in the tropics. Multiple factors, including light, sedimentation, water flow, and predation have been proposed to explain this pattern, but experimental tests of these hypotheses are lacking. We manipulated light level and predation to test whether variation in these mechanisms could be responsible for the shift in composition of sessile communities between vertical and horizontal surfaces in the rocky subtidal Gulf of Maine. Shaded horizontally oriented granite plots were dominated by invertebrates (e.g., ascidians, barnacles, bryozoans) after 25 months. Unshaded plots were dominated by macroalgae, which was virtually absent in shaded plots. Exclusion of grazers with cages had no effect on percent cover of invertebrates or algae. Preferential settlement of invertebrate larvae to shaded plots, due to larval behaviors such as negative phototaxis, did not seem to play a role. Shading likely affects post-settlement mortality of invertebrates by alleviating competition for space with algae, although greater abundance of micropredators in algal-dominated communities could also be important. Communities on shaded plots lacked many taxa present on natural wall communities, likely due to greater disturbance on horizontal substrates and/or lack of sufficient time for colonization of these taxa. These results suggest that light plays a key role in controlling the structure, composition, and function of shallow subtidal communities.