Population Genetics of Marine Organisms
by Dennis Hedgecock
From its inception, U.S. GLOBEC has been concerned with resolving the
systematics and population genetic structures of organisms targeted for
long-term field study. This concern reflects a growing interest on the
part of biological oceanographers and fisheries scientists in the theory
and practice of population genetics, particularly as enhanced by
molecular biological methods. Recent expressions of this interest,
among others, have been the National Science Foundation Fellowships in
Marine Biotechnology, the National Research Council's Ocean Studies
Board planning meeting, "Marine Biodiversity and the Ocean Environment,"
held at the University of California, Irvine, in April 1993, and the
recent symposium at the 1993 CalCOFI Conference, "Genetics of the Fauna
of the California Current." This article is a personal view of exciting
new developments in marine population genetics research and their
application to U.S. GLOBEC.
Major scientific questions being addressed by population geneticists
working on marine animals can be grouped under five headings: (1)
identification of morphologically cryptic, sibling species; (2) amount
and spatial structure of genetic diversity within species; (3) temporal
genetic change; (4) retrospective analyses of historical oceanographic
collections; (5) phylogenetic and phylogeographic analyses; and (6)
development of theory and statistics to aid in the analysis and
interpretation of rapidly accumulating, molecular data.
Sibling Species
A major contribution of population genetic studies to marine biology has
been the identification of biological species within morphologically
defined taxa, including some that are well studied such as Mytilus,
Capitella, and Calanus (reviewed by Knowlton 1993). These discoveries,
which are often serendipitous by-products of research directed at other
questions, could eventually increase marine biodiversity at the species
level by an order of magnitude. A systematic investigation of the
frequency of sibling species in various taxa appears warranted.
Prudence dictates that the taxonomy of all U.S. GLOBEC target organisms
be confirmed by both traditional and molecular methods and that voucher
specimens be kept.
Amount and Spatial Structure of Genetic Diversity within Species
The amount of genetic variation maintained in species is perhaps the most
thoroughly studied aspect of marine population genetics. Early studies
of protein polymorphism documented widely varying levels of genetic
diversity among marine taxa, but causes of this variation are not
entirely clear. Comparative studies of taxa differing in life-history
or ecological traits have provided few compelling general explanations
for the maintenance of different levels of genetic diversity in
different taxonomic groups (Ward et al. 1992). Certainly, the amount of
diversity measured for a particular taxon depends to a great extent on
the particular type and set of genetic markers studied.
Spatial structure of genetic diversity or population subdivision is the
topic of most interest to oceanographers and the U.S. GLOBEC community,
because it is tied to the hope that the geographic sources of
recruitment to marine animal populations might be identified by their
genetic makeup. Indeed, "biotechnology" has in part been sold to this
community as the solution to this important, mass transport problem.
For most species of interest, those that comprise the zooplankton
broadly speaking, this hope is not well founded in logic or fact.
Population genetic theory tells us that dispersal among geographic
populations, even very low levels of dispersal on the order of a few
migrants per generation, can eliminate the very genetic differences
among geographic populations that are supposed to permit identification
of provenance. Early studies of proteins established that species with
dispersing, planktotrophic larvae had, as expected, much less geographic
variation or population subdivision than species with poorly dispersing,
lecithotrophic larvae (Burton 1983). The many genetic studies that have
now been made of fish and invertebrate marine species with
planktonically dispersing larvae have clearly shown them to be
genetically quite homogeneous over very large regions, though not often
over their entire geographic ranges. A common measure of population
genetic differences is FST, the ratio of the variance of allelic
frequencies among localities to the maximum variance that would obtain
if each locality were fixed for one of the alternative alleles without
change in mean allelic frequency. FST is generally much less than 0.05
for marine species with planktonic larvae.
The oceanographer's problem is to detect if a sample of
zooplankton is a genetic mixture and if so, to determine the
contributions of different geographic populations to the mix. This
problem has been solved for certain mixed-stock fisheries, particularly
for anadromous species; sophisticated statistical analysis of genetic
data can identify source populations and their relative contributions to
ocean salmon catches (Utter and Ryman 1993). These methods work well
for salmon because anadramous source populations are identifiable in
space and are genetically distinct, with FST values ranging up to 0.5;
these same methods are not likely to work for the many marine species
that lack obvious spatial genetic structure (Fig. 1).
Identification of sources and sinks of zooplanktonic populations
is critical to understanding their distribution and abundance. It
remains to be seen, however, whether the promise of greater resolution
of individual and population genetic differences afforded by DNA
analyses will make such identifications tractable. The fundamental
limitation may be the dispersal biology of such species, which
homogenizes the frequencies of alleles at all loci, be they DNA
sequences or allozymes.
Nevertheless, studies of spatial genetic variation should be
made for all U.S. GLOBEC target species as a part of a baseline
population genetic description. Such studies may reveal exceptions to
the general rule or they may reveal a previously unrecognized barrier to
dispersal that has resulted in a major genetic subdivision. As a rule,
however, we should not expect such studies to yield conclusive
information about the sources of recruits or the water masses bearing
them.
Temporal Genetic Change
Despite the generalization that marine species with planktonic dispersal
are genetically homogeneous over large geographic regions, statistical
comparisons of allelic frequencies among samples taken sometimes on
scales of meters often indicate significant, "chaotic," microspatial
heterogeneity embedded within the basin-scale similarity of allelic
frequencies. Recent work on this paradox has focused attention on
temporal genetic change in marine populations, which in the few studies
conducted thus far appears to be as large or larger than geographic
variation on basin scales (reviewed by Hedgecock 1994).
Microspatial heterogeneity and temporal change may be jointly explained
by the hypothesis that a large variance in individual reproductive
success results from a sweepstakes-chance matching of reproductive
effort with spatio-temporal windows of oceanographic conditions
conducive to spawning, fertilization, larval survival, and recruitment
(Hedgecock 1994). According to this hypothesis, only small fractions
(from 1/100 to 1/100,000) of spawning adults effectively reproduce and
replace standing adult populations each generation, so that random
genetic drift of allelic frequencies should be measurable in some
populations. This prediction has been borne out by temporal studies of
semi-isolated natural oyster populations. Amounts of genetic drift
imply effective population sizes that are many orders of magnitude less
than the simple abundance of adults. More detailed studies of larval
populations are needed to test a second prediction that specific cohorts
of larvae should show genetic evidence of having been produced by only a
segment of the potential parental pool.
This hypothesis establishes a connection between oceanography and
population genetics in the study of recruitment and may explain how
local adaptations and speciation can occur in seemingly large,
well-mixed marine populations. Temporal genetic studies are therefore
germane to U.S. GLOBEC field studies.
Retrospective Analyses of Historical Collections
An exciting new technology for enzymatically amplifying specific DNA
sequences from small and preserved biological samples, the polymerase
chain reaction or PCR (Saiki et al 1988) can potentially be applied to
the study of preserved material in large historical oceanographic
collections such as those maintained at Woods Hole Oceanographic
Institute and Scripps Institution of Oceanography. Molecular methods
could aid in a more rapid systematic treatment of these collections and
be used to establish genetic histories for particular species of
interest. Geneticists urge that future collections be stored in alcohol
rather than formalin, which can chemically degrade nucleic acids.
Phylogenetics, Phylogeography, and Paleo-oceanography
Molecular genetic analyses are being used to reconstruct genetic
phylogenies at all taxonomic levels and for many phyla. The application
of phylogenetic methods to molecular as well as organismal traits such
as morphology, life history and behavior, will undoubtedly shed new
light on the evolution and systematics of marine organisms. Comparisons
of genetic divergence within and between closely related species across
paleo-oceanographic barriers of known age, such as the arctic land
barrier or the Isthmus of Panama, are useful for calibrating rates of
molecular evolution and reconstructing the history of faunal exchanges.
Ultimately such studies may provide the basis for development of
biotechnological tools for rapid, automated classification of
oceanographic samples and collections.
Within the past decade, the application of phylogenetic approaches to
molecular variation within species has yielded new insights into
population histories and a new conceptual framework for uniting the
traditionally separate disciplines of systematics and population
genetics (Avise et al. 1987). Studies of mitochondrial DNA in several
species living along the Gulf of Mexico and Atlantic coasts of the U.S.
have revealed concordant patterns of major genetic subdivisions. In all
of these species, Gulf haplotypes give way to Atlantic haplotypes across
a previously recognized biogeographical boundary in southeastern
Florida. Gulf and Atlantic haplotypes represent clades that separated
over a million years ago. Thus, "phylogeographic" patterns reflect the
persistence of historical events in the gene pools of organisms. Such
information is relevant to management and conservation efforts and begs
for inter-disciplinary, paleo-oceanographic explanation. U.S. GLOBEC
studies of species in the California Current may well encounter similar
intraspecific, phylogeographic patterns of variation across the
biogeographic boundary at Point Conception.
Data Analysis, Interpretation, and Archiving
Molecular methods are beginning to generate more information than can be
presently handled by theory and statistical methods developed for the
analysis of allozyme or early DNA-RFLP data. As the potential for
resolving genetic individuality at the level of DNA sequences is
realized, identification of relatedness and clustering of individuals
into biologically meaningful groups become challenging problems. Given
the density of population genetic information in the future, such
computations will likely require routine use of supercomputers. There
is need also to develop new theory for gene phylogenies at the
intraspecific level so that the causes of discordant phylogeographic
patterns among different classes of molecular markers can be
interpreted. Finally, genetic and organismal information from U.S.
GLOBEC studies should be entered into perpetual data sets that can serve
as the basis for detecting long-term trends or shifts in biodiversity.
(Dennis Hedgecock is with the Bodega Marine Laboratory, University of
California, Davis, and is a former member of the U.S. GLOBEC Scientific
Steering Committee.)
References
Avise, J.C., J. Arnold, R. M. Ball, Jr., E. Bermingham, T. Lamb, J. E.
Neigel, C. A. Reeb, and N. C. Saunders. 1987. Intraspecific
phylogeography: the mitochondrial DNA bridge between population genetics
and systematics. Annu. Rev. Ecol. Syst., 18, 489-522.
Burton, R. S. 1983. Protein polymorphisms and genetic differentiation
of marine invertebrate populations. Marine Biology Letters, 4, 193-206.
Hedgecock, D. 1994. Does variance in reproductive success limit
effective population sizes of marine organisms? In: Genetics and
Evolution of Aquatic Organisms, A. R. Beaumont (Ed.), Chapman & Hall,
London, pp. 122-134, in press.
Knowlton, N. 1993. Sibling species in the sea. Annu. Rev. Ecol.
Syst., 24, 189-216.
Saiki, R. K., D. H. Gelfand, S. Stoffel, S. J. Scharf, R. Higuchi, G. T.
Horn, K. B. Mullis and E. A. Erlich. 1988. Primer-directed enzymatic
amplification of DNA with a thermostable DNA polymerase. Science, 239,
487-491.
Utter, F. and N. Ryman. 1993. Genetic markers and mixed stock
fisheries. Fisheries, 18, 11-21.
Waples, R. S. and P. E. Smouse. 1990. Gametic disequilibrium analysis
as a means of identifying mixtures of salmon populations. American
Fisheries Society Symposium, 7, 439-458.
Ward, R. D., D. O. F. Skibinski, and M. Woodwark. 1992. Protein
heterozygosity, protein structure, and Taxonomic differentiation.
Evolutionary Biology, vol. 26, M. K. Hecht et al. (Eds.), Plenum Press,
pp. 73-159.
