Joseph E. Neigel

Demographic influences on mitochondrial DNA lineage survivorship in animal populations

SummaryProbability models of branching processes and computer simulations of these models are used to examine stochastic survivorship of female lineages under a variety of demographic scenarios. A parameter II, defined as the probability of survival of two or more independent lineages over G generations, is monitored as a function of founding size of a population, population size at carrying capacity, and the frequency distributions of surviving progeny.Stochastic lineage extinction can be very rapid under certain biologically plausible demographic conditions. For stable-sized populations initiated by n females and/or regulated about carrying capacity k=n, it is highly probable that within about 4n generations all descendants will trace their ancestries to a single founder female. For a given mean family size, increased variance decreases lineage survivorship. In expanding populations, however, lineage extinction is dramatically slowed, and the final k value is a far more important determinant of II than is the size of the population at founding. The results are discussed in the context of recent empirical observations of low mitochondrial DNA (mtDNA) sequence heterogeneity in humans and expected distributions of asexually transmitted traits among sexually reproducing species.

CLONAL DIVERSITY AND POPULATION STRUCTURE IN A REEF-BUILDING CORAL, ACROPORA CERVICORNIS : SELF-RECOGNITION ANALYSIS AND DEMOGRAPHIC INTERPRETATION

Description of genetic variation in a population, recognized by Hubby and Lewontin (1966) as providing the fundamental datum of evolutionary studies, is now routinely accomplished by electrophoretic characterization of allozyme variation and by other molecular techniques. These studies have revealed considerable variation at the molecular level, as well as the structure of this variation within and among populations. Although the value of the molecular approach in population genetics is beyond dispute, there remain interesting aspects of population variation not directly assayable by these methods. Biological self-recognition phenomena, exemplified by self-sterility in flowering plants and immune systems in animals, have been utilized in a population genetic context for only a few species. An analysis of genetic population structure based upon a self-recognition phenomenon requires a relatively straightforward assay incorporating the phenomenon, and an established relationship between the detectable polymorphisms and a more general aspect of population structure. Harberd used a combination of morphological characters and self-sterility relationships to deduce clonal structure in populations of the grasses, Festuca rubra and F. ovina (Harberd, 1961, 1962a) and the clover, Trifolium repens (Harberd, 1962b). In most vertebrate populations nearly every individual possesses a unique histocompatibility type, but some vertebrate population structures have been characterized by a departure from this condition of complete diversification. Kallman (1964) interpreted the occurrence of duplicated histocompatibility types within isolated populations of platyfish as an indication of inbreeding. For populations in which asexual reproduction occurs, some authors (Maslin, 1967; Cuellar, 1976, 1977; Angus and Schultz, 1979; Angus, 1980) have assumed that each clone is distinguished by a unique histocompatibility type, thus equating the diversity of incompatible strains with clonal diversity. In one such study (Angus and Schultz, 1979), a tissue graft analysis applied to populations of the unisexual fish, Poeciliopsis monacha-lucida, resolved more clones than had been detected in an earlier electrophoretic survey (Vrijenhoek et al.,

ESTIMATION OF SINGLE GENERATION MIGRATION DISTANCES FROM GEOGRAPHIC VARIATION IN ANIMAL MITOCHONDRIAL DNA

A new approach is introduced for the analysis of dispersal from the geographic distributions of mtDNA lineages. The method is based on the expected spatial distributions of lineages arising under a multigeneration random walk process. Unlike previous methods based on the predicted equilibria between genetic drift and gene flow, this approach is appropriate for non‐equilibrium conditions, and yields an estimate of dispersal distance rather than dispersal rate. The theoretical basis for this method is examined, and an analysis of mtDNA restriction site data for Peromyscus maniculatus is presented as an example of how this approach can be applied to empirical data.

Gene genealogies within the organismal pedigrees of random-mating populations.

-Using computer simulations, we generated and analyzed genetic distances among selectively neutral haplotypes transmitted through gene genealogies with random-mating organismal pedigrees. Constraints and possible biases on haplotype distances due to correlated ancestry were evaluated by comparing observed distributions ofdistances to those predicted from an inbreeding theory that assumes independence among haplotype pairs. Results suggest that: I) mean time to common ancestry ofneutral haplotypes can be a reasonably good predictor ofevolutionary effective population size; 2) the nonindependence ofhaplotype paths ofdescent within a given gene genealogy typically produces significant departures from the theoretical probability distributions ofhaplotype distances; 3) frequency distributions of distances between haplotypes drawn from replicate organismal pedigrees or from multiple unlinked loci within an organismal pedigree exhibit very close agreement with the theory for independent haplotypes. These results are relevant to interpretations ofcurrent molecular data on genetic distances among nonrecombining haplotypes at either nuclear or cytoplasmic loci. Received October 21, 1988. Accepted November 13, 1989 With the advent of efficient laboratory methods for nucleotide sequencing and restriction-site mapping, it has become feasible to assay many DNA haplotypes at particular loci from a population or species. Such data can be analyzed phylogenetically to estimate the evolutionary relationships (genegenealogies or gene trees [Nei, 1987]) among the alleles of a gene (Avise, 1989). There is now a need for further development of a corresponding theory for haplotype genealogies at the within-species level. A suitable theory should include the expected effects on allelic relationships ofvarious historical demographic factors such as population size and gene-flow pattern. Here we analyze one property of gene genealogies-the distribution of times to common ancestry for haplotypes-within random mating populations. Suppose that, from each of a very large number of replicate, random-mating populations of effective size N e, two haplotypes (alleles) were drawn at random from a nuclear gene locus. Suppose further that the times to common ancestry (the times to identity by descent) ofthese haplotype pairs were determined. In this idealized scenario, the probability f(G) that two randomly chosen haplotypes are derived from the same ancestral haplotype that existed G generations prior is f(G) = (_1_)(1 __1_)G-1 (1) 2Ne 2Ne (Tajima, 1983; Nei, 1987). For a maternally transmitted gene such as mitochondrial DNA (mtDNA) in higher animals, 2Ne in Equation (1) is replaced by Ne(O, the effective size of the female population (Avise et al., 1988). Equation (1) is the probability distribution function of times to identity by descent among independent haplotypes. The form of this distribution is geometric, with mean 2Ne and variance 4Ne2 . In reality, such an empirical sampling design for haplotypes is not practical. Rather, an array ofhaplotypes from one gene (such as alcohol dehydrogenase or mtDNA) is normally assayed from one population or species (e.g., Aquadro et al., 1986; Avise et al., 1987; Kreitman, 1983). While genetic distances among haplotypes can be calculated and converted to a frequency distribution of times to common ancestry using a molecular-clock calibration (Avise et al., 1988), this distribution need not agree with the above theory because (among other possibilities) the haplotype distances are correlated due to coancestry through a particular gene genealogy within an organismal pedigree. In this paper, we employ computer sim-

TESTS OF PHYLOGEOGRAPHIC MODELS WITH NUCLEAR AND MITOCHONDRIAL DNA SEQUENCE VARIATION IN THE STONE CRABS, MENIPPE ADINA AND MENIPPE MERCENARIA

Evolutionary relationships among stone crabs (Menippe) from the Gulf of Mexico and western Atlantic were investigated by comparisons of restriction sites within anonymous nuclear DNA sequences and nucleotide sequences of both mitochondrial and a duplicated nuclear form of the mitochondrial large subunit ribosomal RNA (LSrDNA) gene. A survey of over 100 restriction sites by Southern blot analysis with 10 anonymous nuclear DNA sequence probes failed to reveal any differences between Menippe adina and M. mercenaria. Sequence comparisons of both mitochondrial and nuclear forms of the LSrDNA gene also did not distinguish these species. Although both LSrDNA gene sequences were variable, some haplotypes were shared by the two species, implying either incomplete gene lineage sorting or introgressive hybridization. Based on molecular clock calibrations, we estimate that all of the observed mitochondrial LSrDNA sequences share a common ancestor between 1.5 and 2.7 million years before present (M.Y.B.P.). However, because identical sequences are shared by the two species, these data are also compatible with a more recent common ancestry. These findings conflict with a previously proposed biogeographic scenario for North American Menippe, which featured a relict hybrid zone on the Atlantic Coast. We suggest an alternative scenario based on relatively recent events and ongoing, rather than historical, gene flow.

Phenotypic variation within histocompatibility-defined clones of marine sponges

Nongenetic phenotypic variation can be identified by its occurrence within genetically uniform clones. A histocompatibility bioassay of clonal identity was used to ascertain the extent of phenotypic variation within natural clones of two species of marine sponges. Multiple morphological forms of the sponge Aplysina fistularis were found to occur within single clones, indicating a nongenetic polymorphism. In contrast, a genetic basis is suggested for a polymorphism of Aplysina cauliformis; within single clones of this species, individuals were uniform in color and morphology.

The precision of histocompatibility response in clonal recognition in tropical marine sponges

Recently discovered histocompatibility‐like phenomena in sponges (Phylum Porifera) have prompted attempts to measure the precision with which allogeneic grafts are recognized and rejected. The results of these investigations have been extremely varied, ranging from suggestions that allorecognition does not occur to suggestions that every genetically distinct individual may be unique in histocompatibility type. Interpretation of these findings is complicated by the variation in methods and species used by different workers. Here we compare various measurements of allorecognition precision for several species of tropical marine sponges. From our results we conclude that 1) tissue implant grafts are more prone to artifact than grafts between intact sponges; 2) the possibility of clonal propogation should be considered when graft acceptances are observed between sponges selected from a single population; and 3) allozyme variation in Niphates erecta shows that occasional grafts between genetically different individuals may be accepted.

ENHANCING THE RETRDEVABILITY OF POPULATION GENETIC SURVEY DATA? AN ASSESSMENT OF ANIMAL MITOCHONDRIAL DNA STUDIES

Surveys of genetic variation in natural populations represent a valuable and often irreplaceable resource. It may be desirable to reanalyze data as new methods are developed for comparisons with other populations or for comparisons with the same populations at different times. We evaluated existing mechanisms of data preservation in a survey of 627 published surveys of mitochondrial DNA variation in animal and found that over half of the datasets (56%) contained insufficient information for reanalysis. In many cases, publication of complete data would not have added excessively to the length of the publication. Because at present, publications represent the main archive of population genetic data, we offer recommendations for how the essential data from mtDNA surveys can be presented in a form that is complete and concise.