David W. Foltz

GENETIC EVIDENCE FOR LONG-TERM MONOGAMY IN A SMALL RODENT, PEROMYSCUS POLIONOTUS

Populations of Peromyscus polionotus, the oldfield mouse, are organized into family groups which are characterized by a high degree of monogamy. There is no evidence that females of this species ever mate with more than one male for each litter. Females that are collected in the field with males have the same mate for consecutive litters (the frequency of mate switching for these females does not differ significantly from zero). In addition, the male that is collected with the female is usually the father of her offspring (the frequency of nonpaternity is .117). Thus, oldfield mice are overwhelmingly monogamous. However, a few females may not form long-term monogamous relationships, as shown by the relatively high frequency of mate switching for females collected without males (.40). Recent research has uncovered several other probable cases of monogamy among small rodents. Any generalization about mating systems among mammals must consider the diversity of mating systems among small rodents. The methods used in this paper have generality and could be used to study the mating system in other mammals that are difficult or impossible to study by direct observation.

Null alleles as a possible cause of heterozygote deficiencies in the oyster Crassostrea virginica and other bivalves

Populations of several marine bivalves exhibit significant deficiencies of heterozygotes (compared with the Hardy-Weinberg expectations) at some allozyme loci (Berger, 1983; Singh and Green, 1984; Zouros and Foltz, 1984). These deficiencies have usually been explained by invoking nonrandom mating, selection, or population structure (Wahlund effect). Less attention has been paid to the possibility that the deficiencies are due to the occurrence of null (nonreactive) alleles or to other factors causing allozyme loci to depart from a simple codominant model of genetic control. Null alleles may lead to heterozygote deficiencies if null heterozygotes are mistakenly scored as active homozygotes. Only a few studies have reported on inheritance of allozyme phenotypes in progeny from pair crosses

Amplification dynamics of human-specific (HS) alu family members

We have investigated the distribution of several recently inserted Alu family members within representatives of diverse human groups. Human population studies using 65 unrelated human DNA samples, as well as a familial study to test inheritance, showed that individual Alu family members could be divided into three groups. The first group consisted of relatively older Alu family members which were monomorphic (homozygous) throughout the population tested (HS C3N1 and C4N6). The second group (HS C4N2, C4N5 and C4N8), apparently inserted into other repetitive regions of the genome, resulting in inconclusive results in the PCR test used. However, it is clear that these particular Alu insertions were present in a majority if not all of the loci tested. The third group was comprised of three dimorphic Alu family members (HS C2N4, C4N4 and TPA 25). Only a single Alu family member (TPA 25) displayed a high degree of dimorphism within the human population. This latter example also showed different allele frequencies in different human groups. The isolation and characterization of additional highly dimorphic Alu family members should provide a useful tool for human population genetics.

Genetic population structure of a species' complex of blue mussels (Mytilus spp.)

Blue mussels representing two nominal species (Mytilus trossulus Gould, 1850 and Mytilus galloprovincialis Lamarck, 1819 were collected from 28 intertidal locations along the Pacific coast of the USA in 1990–1991 (total N=1255) and examined for variation at 15 allozyme loci. Twelve samples, mostly from a region of suspected hybridization, were analyzed for variation in seven shell characters. Principal-components analysis of allozyme data revealed three groups based on first principal-component scores, which were identified as M. trossulus, M. galloprovincialis, and hybrids. Canonical discriminant analysis of shell characters was less successful in separating mussels into discrete groups. Each location was characterized for four environmental variables: (1) temperature, (2) salinity, (3) tidal height and (4) degree of exposure to wave action, which were then used as independent variables in a series of multiple-regression analyses, with the proportions of the two species as dependent variables. Temperature and salinity had significant (P<0.05) effects on the macrogeographic distribution of the two species, whereas the effects of height in the tidal zone and degree of wave exposure were not statistically significant. Salinity was found to have a greater influence than temperature on the microgeographic distribution of the two species. M. trossulus was more abundant at locations with lower temperatures and greater salinity variation than M. galloprovincialis. The two species appear to be ecologically distinct, and their genetic integrity is at least partly the result of environmental heterogeneity.

DO BLACK-TAILED PRAIRIE DOGS MINIMIZE INBREEDING ?

Considerable controversy surrounds the importance of inbreeding in natural populations. The rate of natural inbreeding and the influences of behavioral mechanisms that serve to promote or minimize inbreeding (e.g., philopatry vs. dispersal) are poorly understood. We studied inbreeding and social structuring of a population of black‐tailed prairie dogs (Cynomys ludovicianus) to assess the influence of dispersal and mating behavior on patterns of genetic variation. We examined 15 years of data on prairie dogs, including survival and reproduction, social behavior, pedigrees, and allozyme alleles. Pedigrees revealed mean inbreeding coefficients (F) of 1–2%. A breeding‐group model that incorporated details of prairie dog behavior and demography was used to estimate values of fixation indices (F‐statistics). Model predictions were consistent with the minimization of inbreeding within breeding groups (“coteries,” asymptotic FIL = –0.18) and random mating within the subpopulation (“colony,” asymptotic FIS = 0.00). Estimates from pedigrees (mean FIL = –0.23, mean FIS = 0.00) and allozyme data (mean FIL = –0.21, mean FIS = –0.01) were consistent with predictions of the model. The breeding‐group model, pedigrees, and allozyme data showed remarkably congruent results, and indicated strong genetic structuring within the colony (FLS = 0.16, 0.19, and 0.17, respectively). We concluded that although inbreeding occurred in the colony, the rate of inbreeding was strongly minimized at the level of breeding groups, but not at the subpopulation level. The behavioral mechanisms most important to the minimization of inbreeding appeared to be patterns of male‐biased dispersal of both subadults and adults, associated with strong philopatry of females. Incest avoidance also occurred, associated with recognition of close kin via direct social learning within the breeding groups.

Breeding Groups and Gene Dynamics in a Socially Structured Population of Prairie Dogs

Genetic substructuring of a colony of black-tailed prairie dogs ( Cynomys ludovicianus ) was examined using three different sources of information: allozyme alleles, pedigrees, and demography (a “breeding-group” model based on mating and dispersal patterns). Prairie dogs and their social breeding groups (called “coteries”) were studied under natural conditions during a 15-year period. Prairie-dog coteries exhibited substantial genetic differentiation, with 15–20% of the genetic variation occurring among coteries. Mating patterns within the colony approximated random mating, and, thus, mates tended to originate from different coteries. Social groups of black-tailed prairie dogs resulted in genetic substructuring of the colony, a conclusion that was supported by estimates from allozyme alleles and colony pedigrees. Predictions of the breeding-group model also were consistent with and supported by estimates from allozyme and pedigree data. Some methodological problems were revealed during analyses. Although individuals of all ages usually are pooled for biochemical estimates of among-group genetic differentiation, our estimates of among-coterie variation from allozyme data were somewhat higher for young than for older prairie dogs, perhaps due to sampling effects caused by mating patterns and infanticide of offspring. Pedigree estimates of among-coterie genetic differentiation were significantly positive for young prairie dogs, adult females, and adult males. Those estimates were always more accurate for the offspring generation, however, because pedigree data were always more complete for young and genetic differences among coteries were diluted by virtually complete dispersal of males away from their natal coteries.

Population genetics and systematics of the Leptasterias hexactis (Echinodermata: Asteroidea) species complex

Morphological characters and 14 enzyme loci were examined for 1 040 sea stars, currently recognized as forms ofLeptasterias hexactis, from Lynn Canal, Alaska, and Puget Sound, Washington, USA, between March 1988 and April 1989. Three morphologically and two genetically distinctLeptasterias forms were identified. The most common form found at both localities wasL. epichlora (Brandt)sensu Verrill.L. hexactis (Stimpson)sensu Verrill co-occurred withL. epichlora at all study sites and apparently hybridizes extensively withL. epichlora in the Puget Sound region, but rarely, if at all, in Alaska. The presumptive product of this hybridization morphologically resembledL. aequalis (Stimpson)sensu Fisher, and was conspicuously absent from Alaskan samples. Considerable genetic distance existed betweenL. epichlora andL. hexactis (NeisD=0.19±0.01) and moderate genetic differentiation occurred between populations of each species from Alaska and Washington (Weir and CockerhamsFRT=0.29±0.04 forL. epichlora and 0.21±0.15 forL. hexactis). A significant (p<0.05) deficiency in the proportion of heterozygous individuals was found compared to Hardy-Weinberg expectations (Wrights fixation index,FID=0.12±0.04 and 0.31±0.08 forL. epichlora andL. hexactis, respectively). However, mean observed heterozygosity for each species (0.09±0.03, 0.14±0.04 and 0.14±0.04 forL. epichlora, L. hexactis andL. aequalis, respectively) fell within the range of reported values for other asteroid species (ca. 0.04 to 0.37). The results of this study indicate that considerable genetic integrity is maintained betweenL. epichlora andL. hexactis, which warrants their recognition as distinct species despite their apparent hybridization in the Puget Sound region.

GENETIC EVIDENCE OF OUTBREEDING IN THE BLACK-TAILED PRAIRIE DOG (CYNOMYS LUDOVICIANUS)

The study of mating systems and the effect of social behavior on the genetic structure of animal populations is an important topic in evolutionary biology. The theoretical approaches of Wright (1978 and references therein) and Malecot (1969) have been extended by many other researchers, including Cockerham (1973), Jacquard (1974), Smith (1974) and Nei (1977). Two methods have been used to study mating systems in natural populations. The more usual approach is to assay the genetic structure by collecting a population sample and determining allele and genotype frequencies at one or more polymorphic loci. The number of such studies has increased rapidly in recent years, due to the now-routine application of gel electrophoresis in population biology. Previous research on the genetic structure of rodent populations includes that of Petras (1967), Selander (1970), Birdsall and Nash (1973), Myers (1974), Schwartz and Armitage (1980, 1981), Foltz (1981), Hanken and Sherman (1981) and Patton and Feder (1981). A second approach involves the analysis of pedigrees obtained by long-term study of populations whose members are individually marked. Because of the ob-vious difficulties in obtaining this information for natural populations, such studies are relatively rare. Exceptions include the work of Howard (1949), Bulmer (1973), Missakian (1973), Greenwood et al. (1978) and Brown and Brown (1981).

Segregation and linkage studies of allozyme loci in pair crosses of the oysterCrassostrea virginica

The genetic control of 11 electrophoretically detected allozyme polymorphisms in the oysterCrassostrea virginica was investigated in 10 pair crosses. For nine allozyme loci, each offspring shared at least one band (electromorph) with each parent. For the remaining two loci (mannosephosphate isomerase and leucine aminopeptidase-2), some offspring failed to share a band with one or both parents. Several lines of evidence indicated that these anomalous results were due to transmission of null alleles. There was evidence of distorted segregation at 8 of the 11 loci. The departures from the Mendelian expectations within the pair crosses might be due either to viability selection in the offspring or to gametic selection in one or both parents, although the possibility that the distortion is due to a locus linked to the allozyme locus cannot be ruled out. However, there was no evidence that heterozygosity per se had an effect on viability of offspring within a cross. Linkage analysis revealed two linkage groups, one consisting of four allozyme loci and the other consisting of three loci.

Genetics and taxonomy of ribbed mussels (Geukensia spp.)

Ribbed mussels (232 in all) representing the nominal species Geukensia demissa (Dillwyn, 1817) were collected at nine coastal North American locations (two Pacific, four Atlantic and three Gulf Coast locations) between January 1990 and September 1991, and examined for nine shell characters and for variation at 18 allozyme loci. Two genetically-differentiated groups were identified and called demissa-type and granosissima-type mussles, based on similarity of geographic range to previously recognized subspecies of G. demissa. There was very little genetic differentiation of populations over moderate to large (3000 km) distances along the Atlantic coast (for demissa-type mussels), along the Gulf Coast (for granosissima-type mussels), or between Pacific and Atlantic populations of demissa-type mussles. The two types of mussels were differentiated genetically (Neis unbiased genetic distance =0.55±0.20) at a level characteristic of separate species in other molluscan taxa, and to a lesser extent were differentiated morphologically. We recommend that the two types of mussels be treated as separate species within the genus Geukensia: G. demissa (Dillwyn, 1817) and G. granosissima (Sowerby, 1914).