ACHIEVEMENTS IN EVOLUTIONARY MARINE BIOLOGY

prepared by S. R. Palumbi and J. B. C. Jackson

Overview - the pattern of oceanic diversity

The most important biological insights stem from the realization that biological diversity in the sea has been seriously underestimated at every level of biological hierarchy from the genetic level to the species level to the community and ecosystem levels. These increases do more than simply add bulk to the world's species list. They suggest that evolutionary processes that generate species, or that generate and maintain differentiation within species, are occurring on temporal and spatial scales that are much shorter than previously assumed. In addition, evolutionary changes are now known to be characterized by marked discontinuities over time (e.g. long stasis followed by fast morphological evolution) or over space (e.g. large species ranges punctuated by concordant biogeographic and genetic boundaries).

What aspects of the physical or biological environment delineate temporal or geographic discontinuities? Do modern physical oceanographic features determine the limits of marine populations? To what extent does the environmental history of the Pleistocene affect modern marine communities? These questions combine evolutionary history and modern oceanography to paint an integrated picture of the environmental biology of the sea.

The numbers of marine species, even of well studied taxa, are many times greater than realized two decades ago. Major groups of microorganisms that were virtually unknown in the sea are now known to be important components of the marine biosphere. Populations of marine species are more subdivided genetically than realized before, leading to an increasing search for the processes generating interpopulation genetic diversity. This newly documented diversity and discontinuity has profound implications for understanding the origins and maintenance of biodiversity in the sea, the generality of ecological interactions, and ecosystem function.

Evolution is not merely a process that generated past diversity, or that slowly alters species and communities. It also acts in the present day to change the nature of species in modern oceans. Fisheries exploitation has resulted in the evolution of slower growing fish with smaller reproductive sizes. Coastal habitat perturbation has resulted in the planktonic dominance of different species best characterized as oceanic weeds. Other perturbations may be having effects on open ocean communities. Has increased nitrogen input to the oceans changed planktonic physiological attributes or community composition? Such questions are fundamental to understanding of oceanic assemblages and how they interact over varying spatial and temporal scales.

Below we divide achievements in evolutionary biological oceanography very broadly into those studies concerned with spatial pattern in modern taxa and those concerned with temporal patterns in fossil assemblages. In both, links between organismal life history traits and ecological patterns are apparent. Both also suggest that evolution in the sea is not gradual or clinal, but is highly dynamic and punctuated. These dynamic, punctuated responses are apparent in the historic record of the marine communities derived from fossil assemblages and from analyses of genetic structure of persistent populations. They imply that non-linear ecological and evolutionary responses are a hallmark of oceanic ecosystems, and that such non-linear responses to current global change can be expected.

Achievements in genetics and population biology: the long and the short of it

1) 1) Simple observations by Rudy Scheltema and colleagues have shown repeatedly that the larvae of coastal marine invertebrates can be found in abundance 1000's of km from any shore line and far from any adult population. These larvae have been shown to be capable of metamorphosing into adults, and provide a long-distance dispersal mechanism that is equaled only by microscopic animals, spores and seeds traveling the atmospheric jet stream. By extension, many marine species are thought to have high dispersal potential (even if their larvae are not caught by open-water plankton tows), and this has engendered a view of ocean populations as demographically open over large spatial and temporal scales. Data from studies of genetic variation have in many cases confirmed the view that marine populations have a large amount of realized dispersal. Many marine species have very low genetic differentiation over large spatial scales, and species with lower dispersal potential tend to show a finer genetic mosaic over shorter spatial scales.

2) The genetics of population differentiation reveals contradictions about dispersal. Recent genetic and biogeographic evidence shows that the view of marine population structure expressed in #1, above, is too simplistic. Although larval dispersal potential appears sufficient to prevent differentiation in some instances, there are other instances in which abrupt genetic or community transitions occur. These stunning exceptions to the easy 'long-dispersal' generalization demand a different paradigm of marine population structure. The strongest demonstration of the need for a different paradigm comes from intensive study of the genetic of marine populations along the SE coast of the US. Here, John Avise and colleagues have shown there to be strong genetic differentiation of marine populations separated by only 10's - 100's of km. The American oyster Crassostrea virginica shows a shift in mitochondrial and nuclear genetic markers over only a 20 km stretch of coastline in northern Florida. Many other species including other bivalves, crabs, and fishes show a similar pattern. These genetic breaks correspond to a well-known biogeographic break along this coast line. The surprise is that these genetic differences, no matter how they originally arose, are not wiped out by long distance marine dispersal. Because they are not eroded by this mechanism, the generalized view of open marine populations with wide-spread demographic exchange can not be operating for these species. Even taxa with widespread larvae seem to show evidence of such historical divisions across this region, creating marked geographic discontinuities in the genetics of highly dispersive, continuously distributed species.

Which view is correct: Long dispersal by drifting marine larvae or short effective dispersal limited to particular biogeographic zones? The dichotomy applies to all marine species, including open water planktonic forms like copepods, coastal marine fish and invertebrates and drifting algal mats. Probably both patterns of dispersal occur across the same environmental mosaics, but we have scant theoretical framework with which to predict the outcome for particular species. Although not enough comparative data are available to completely understand global patterns, it is becoming clearer that within a given species, long distance dispersal often occurs over some parts of the range (leading to broad genetic homogeneity) whereas across other parts of the range, genetic discontinuities can exist over very short spatial scales. The dynamics of these discontinuities (do they remain stable in space? time?) are largely unknown, as are the physical and biological environments that allow them to exist. In addition, not all biogeographic boundaries have the same effect on genetic patterns. The province boundary at Point Conception, California marks the transition between Californiana and Oregonia biogeographic zones, but this major boundary does not appear to be a genetic break. What is different about the SE and SW coasts of North America that would account for this profound difference in biological pattern?

3) How many species are in the sea? The oceans are home to vast numbers of species whose existence was not even suspected two decades ago. From a bare bones conception of marine biodiversity, genetic, morphological and physiological data have shown that many oceanic habitats house an astounding number of different species. A treasure trove of marine bacteria have been discovered through abandonment of traditional culture-then-describe approaches. An enormous biomass of microbes with unusual metabolic requirements (e.g. methanogens, thermophiles, etc.) has been discovered as a result. Associated with these are a largely undescribed sea of bacteriophage viruses. Habitats in the deep sea are now known to harbor species diversities on par with the most diverse tropical rainforests or coral reefs. Even well-known shallow water fish and invertebrate taxa are now known to be made up of a larger than anticipated number of very closely related sibling species. The recognition of these species has depended on application of new genetic techniques that reveal subtle genetic distinctions, and on careful taxonomic re-assessments that reveal overlooked morphological or life history distinctions. The need for this careful scrutiny often derives from the recent formation and relatively small genetic distances of these new species.

The evolutionary integrity of these species appears to be maintained by a number of different mechanisms of reproductive isolation (including those that hinge on the recognition of potential mates by adults or even gametes) that operate to limit hybridization of sibling species. Thus, the oceans are populated by a vast array of relatively new species, ones that have evolved under marine conditions prevalent during the Pleistocene and late Pliocene. Although the oceans also harbor living fossils like the horseshoe crab, speciation and extinction operate over relatively rapid time scales to continuously modernize marine taxa. Paleontological evidence (see below) suggests these bouts of speciation and extinction are clustered in time. Data from gene sequence studies tends to corroborate this by frequently showing the derivation of a number of morphologically similar species from a single common ancestor in small bursts of cladogenesis.

The discovery of previously unknown species diversity in the sea requires reassessment of our understanding of the way oceanic ecosystems are organized and how these ecosystems relate to the physical environment. Bacteria and their predators (bacteriophage viruses) are now known to be abundant in sea water, with sometimes over 10,000,000 individuals per ml. These two sets of organisms therefore represent two potentially critical yet previously unsuspected trophic levels in marine ecosystems. Coral bleaching and it's relationship to environmental change is complicated by the complexity of zooxanthella communities now known to inhabit individual corals. Algal blooms, especially those producing toxins, have been an increasing feature of perturbed coastal habitats. How many species are represented by this collection of oceanic weeds? Can we understand the biology of algal blooms without knowing the answer to this question?

The rise in our appreciation for the levels of marine biodiversity and the temporal and spatial scales over which this diversity is generated has obvious implications for our understanding of the stability of marine populations over time, the reconstitution of communities after disruption, and the ability of marine species to adapt to particular environments. They also show that species specific characteristics like life histories or larval behavior can play a basic role in determining crucial biological patterns and that ignoring species identity in describing oceanic processes is a fundamental error.

Hard as rocks - the contribution of paleontologists

The major contribution of paleontology is the discovery that, like the spatial pattern of genetic and biogeographic change, communities and ecosystems change non-linearly and episodically with comparative stasis in between. Profound temporal discontinuity of ecological and evolutionary change is the historical legacy of the newly discovered spatial and taxonomic discontinuity summarized above for recent seas.

4) The great majority of well studied cases of speciation in the fossil record closely match the predictions of the controversial theory of Punctuated Equilibrium, although this does not require acceptance of any radical new evolutionary mechanisms as is commonly supposed. More than 90% of benthic species studied, and about two thirds of planktonic species, exhibit morphological stasis over millions of years with no net change. This does not mean there is no evolution or selection during stasis but that evolution during this period does not lead to new morphospecies. Significant morphological change occurs during cladogenesis with common persistence of unchanged ancestral species. This implies that species-specific patterns of development and behavior also change rapidly at speciation. Strong evidence for this hypothesis comes from the larval shells of hundreds of species of fossil and recent gastropods that, from their first appearance in the fossil record, differ entirely from their putative ancestors in mode of larval development, without evidence of intermediate forms. These fossil insights have recently been confirmed among extant taxa by the demonstration of rapid changes in early development among sister species leading to ecologically different dispersal potential.

In practical terms, testing the Punctuated Equilibrium hypothesis requires the demonstration that temporal changes in morphology within a species are so small that they cannot account for morphological differences between ancestors and descendants. This in turn requires good preservation, morphometrics and taxonomy to analyze morphological change and discriminate species, with genetic support for the biological significance of living morphospecies. Genetic analyses of mollusks, bryozoans, corals and foraminifera have consistently supported the very fine discrimination of species as discussed above. This has been critical, because apparently gradual patterns of evolutionary change in the sea have consistently turned out to be punctuated after the discovery of cryptic species (this is even the case for G.G. Simpson's celebrated analysis of gradual evolution of horses). In addition, sampling must be very extensive in space and time, and the stratigraphy and age dating precise, in order to be able to distinguish ecological shifts due to climate change from evolution.

All or most of these criteria have been met for more than 100 recent taxa and their ancestors. Among these, virtually all the living species that have a good fossil record originated 1-2 million years ago or more, when environmental conditions in the sea were very different from now. This fact, coupled with the observation of no net change during stasis, implies that local adaptation very rarely leads to speciation, and that the potential for species to respond evolutionarily to changes in their environment is severely limited except under very unusual circumstances. This further implies that we should not expect a gradual evolutionary response to global climate change, but instead a strongly nonlinear response of stasis and thresholds of change. There are very strong limits to the potential for adaptation under most circumstances.

5) Rates of speciation and extinction vary with presumably adaptive variations in life history and development as well as phylogenetic constraints. Species of fossil gastropods with planktonic development are typically more widely distributed geographically, survive longer, and are less prone to speciation and extinction than those with direct development; and the same is true for any eurytopic mollusks that are widely distributed. However, analyses of mass extinctions show that differences in life histories among species within the same higher taxon become less important for speciation and extinction as the intensity of environmental perturbations increase. Moreover, different higher taxa may respond to environmental changes during mass extinction events in very different ways, as is being documented for Caribbean reef corals, bryozoans and mollusks at the end of the Pliocene. Species in different higher taxa also vary greatly in their rates of speciation and extinction in ways that parallel their overall diversity. This is readily understandable for groups with complex behavior and potential for strong sexual selection, such as most fishes and crustaceans, compared to acephalic sessile benthos. But such mechanisms cannot explain differences among groups such as echinoids, reef corals and clams, unless the species specificity of their gamete recognition mechanisms vary widely in their evolutionary potential.

6) Evidence is increasing that speciation and extinction occur mostly in pulses of a million years or less that are correlated with climatic and oceanographic change, with comparative evolutionary quiescence over many millions of years in between. Community composition also changes during such evolutionary pulses or turnover events, but is more stable than expected by chance during the intervals between pulses. The actual percentage of all speciation and extinction that occurs during pulses has been compiled for very few groups. Perhaps the best data are for Caribbean reef corals at the end of the Pliocene which underwent a 75% turnover in species composition in about 1 million years. There was also a profound ecological reorganization of shallow Caribbean reefs to dominance by large elkhorn and staghorn acroporids instead of tiny finger corals. There is also considerable controversy about cause and effect during pulses because it is difficult to precisely correlate biological change with any specific climatic event; although this is exactly what one would expect if evolution occurs as a threshold effect, as implied by Punctuated Equilibrium, rather than by gradual change. A good example is the fierce debate about the role of climate change for evolution of our own genus Homo in Africa, and the same is true for the turnover of corals and mollusks at about the same time in the Caribbean.

For further reading:

Avise JC, 1994. Molecular markers, Natural History, and Evolution. New York: Chapman and Hall.

Jablonski D, 1986. Background and mass extinctions: The alternation of macroevolutionary regimes. Science 231:129-133.

Jackson JBC, Jung P, Coates A, and Collins LS, 1993. Diversity and extinction of tropical american mollusks and emergence of the Isthmus of Panama. Science 260:1624-1626.

Knowlton N, 1993. Sibling species in the sea. Ann. Rev. Ecol. Syst. 24:189-216.

Scheltema RS, 1986. On dispersal and planktonic larvae of benthic invertebrates: An eclectic overview and summary of problems. Bulletin of Marine Science 39:290-322.

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