Evolution of sexual isolation in laboratory populations: fitness differences between mating types and the associated hybrid incompatibilities

Drosophila melanogaster is known to have two races in the incipient stages of speciation that exhibit strong asymmetric premating isolation: Zimbabwe (Z) and cosmopolitan (M). In a study examining the phenotypic and genotypic evolution after secondary contact, we found that despite strong sexual selection favoring the Z-type behavior, it is the M-type behavior that comes to dominate hybrid populations. This article examines the fitness costs associated with the Z-type behavior. We have discovered that these costs are great enough to explain the failure of the Z-type behavior to prosper. Here we report that Z-type females produce approximately half the number of offspring that M-type females produce. Furthermore, crosses between populations have revealed that Z-type females mated to M-type males have approximately 20% fewer offspring than the reciprocal crosses because of an inability of M-type sperm to successfully fertilize Z-type eggs. Hybrid crosses also exhibit much-reduced numbers of viable offspring in addition to reduced hybrid male fertility. These fitness effects suggest that multiple mechanisms of postmating isolation have evolved concurrently with the divergence in behavior.     

Comparison of the chemical, physical, and survival properties of normal and Z-variant alpha-1-antitrypsins.

A procedure has been developed for the purification of Z-type alpha-1-antitrypsin (alpha-1-AT) which is rapid, gentle, and results in good yields. From 4 units (750 ml) of fresh human plasma, obtained from two individuals possessing the Pizz phenotype, 53 mg of pure Z-type alpha-1-AT was obtained. The preparation was homogeneous by the criteria of polyacrylamide gel electrophoresis, both in the presence and absence of sodium dodecyl sulfate, and by analytical ultracentrifugation. When compared to pure alpha-1-AT from plasma of individuals possessing the normal PiMM phenotype, the two proteins were indistinguishable with respect to amino acid composition, sedimentation coefficient (s20w of 3.33 for both M and Z), molecular weight (51,000 by sodium dodecyl sulfate gel electrophoresis and 47,000 by sedimentation equilibrium for both M and Z), and trypsin-combining ratio (0.91 for Z and 0.99 for M). The only difference which was observed between the variant forms of alpha-1-AT was in the carbohydrate composition. The Z-type alpha1-AT contains between 20 and 25% less carbohydrate than the M-type alpha-1-AT. Specifically, the Z-type alpha-1-AT is deficient in 1 glucosamine residue, 3 neutral sugar residues (1 mannose and 2 galactose), and 2 sialic acid residues. Although the Z-variant is deficient in sialic acid, its survival time in the serum of a rabbit was not significantly different from that of M-type alpha-1-AT.     

Incipient Speciation by Sexual Isolation in Drosophila Melanogaster: Extensive Genetic Divergence without Reinforcement

The collection of Drosophila melanogaster from Zimbabwe and nearby regions (the Z-type) yield females who would not mate with the cosmopolitan D. melanogaster males (the M-type). To dissect the genetic basis of this sexual isolation, we constructed 16 whole-chromosome substitution lines between two standard Z-and M-lines. The results were as follows: (1) All substitution lines appear normal in viability and fertility in both sexes, indicating no strong postmating isolation. (2) The genes for the behaviors are mapped to all three major chromosomes with the same ranking and comparable magnitude of effects for both sexes: III > II >> X >/= 0 (III, II and X designate the effects of the three chromosomes). The results suggest less evolution on the X than on autosomes at loci of sexual behavior. (3) The genes for ``Z-maleness' are many and somewhat redundant. Whole-chromosome effects for Z-maleness appear nearly additive and show little dominance. (4) In contrast, ``Z-femaleness' has less redundancy as partial genotypes never exhibit full phenotypic effects. Epistatic interactions and incomplete dominance can sometimes be detected. (5) The extensive genetic divergence underlying sexual isolation has evolved in the absence of detectable reduction in hybrid fitnesses. Sexual selection has apparently been a driving force of multiple facets of speciation at the nascent stage without reinforcement.     

Genetic structure of the global population of banana black leaf streak fungus, Mycosphaerella fijiensis

The genetic structure of Mycosphaerella fijiensis populations around the world was examined using DNA restriction fragment length polymorphism (RFLP) markers. Allele frequencies at 19 nuclear RFLP loci were estimated in a sample of 136 M. fijiensis isolates from five geographical populations representative of banana-producing areas (South-East Asia including the Philippines and Papua New Guinea, Africa, Latin America and Pacific Islands). Within each population, gametic disequilibrium tests between the 19 nuclear RFLP loci were mainly non significant ( P > 0.05), indicating that random sexual reproduction occurred in these populations. All M. fijiensis populations had a high level of genotypic and allelic diversity ( H , gene diversity: 0.25–0.59). The highest levels of gene diversity were found in the two South-East Asian populations ( H : 0.57 and 0.59). Most of the alleles (> 88%) detected in Africa, Latin America and Pacific Islands populations were also detected in South-East Asian populations. Furthermore, a high and significant ( P < 0.05) level of genetic differentiation was observed among M. fijiensis geographical populations (overall estimate of F_st : 0.32). These results were consistent with the hypothesis that M. fijiensis originated in South-East Asia and spread recently to other parts of the world. The level of allelic diversity in M. fijiensis populations from regions other than South-East Asia was drastically reduced, indicating founder effects. The data also suggested rare occurrence of migration of M. fijiensis between continents.     

Phenotypic plasticity of mate recognition systems prevents sexual interference between two sympatric leaf beetle species

Maladaptive sexual interactions among heterospecific individuals (sexual interference) can prevent the coexistence of animal species. Thus, the avoidance of sexual interference by divergence of mate recognition systems is crucial for a stable coexistence in sympatry. Mate recognition systems are thought to be under tight genetic control. However, we demonstrate that mate recognition systems of two closely related sympatric leaf beetle species show a high level of host‐induced phenotypic plasticity. Mate choice in the mustard leaf beetles, Phaedon cochleariae and P. armoraciae, is mediated by cuticular hydrocarbons (CHCs). Divergent host plant use causes a divergence of CHC phenotypes, whereas similar host use leads to their convergence. Consequently, both species exhibit significant behavioral isolation when they feed on alternative host species, but mate randomly when using a common host. Thus, sexual interference between these syntopic leaf beetles is prevented by host‐induced phenotypic plasticity rather than by genotypic divergence of mate recognition systems.     

Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsora lini

Many pathogens undergo both sexual and asexual reproduction to varying degrees, yet the ecological, genetic and evolutionary consequences of different reproductive strategies remain poorly understood. Here we investigate the population genetic structure of wild populations of the plant pathogen Melampsora lini on its host Linum marginale , using amplified fragment length polymorphism (AFLP) markers, two genes underlying pathogen virulence, and phenotypic variation in virulence. In Australia, M. lini occurs as two genetically and geographically divergent lineages (AA and AB), one of which is completely asexual (AB), and the other able to reproduce both clonally and sexually (AA). To quantify the genetic and evolutionary consequences of these different life histories, we sampled five populations in each of two biogeographical regions. Analysis of AFLP data obtained for 275 isolates revealed largely disjunct geographical distributions for the two different lineages, low genetic diversity within lineages, and strong genetic structure among populations within each region. We also detected significant divergence among populations for both Avr genes and virulence phenotypes, although generally these values were lower than those obtained with AFLP markers. Furthermore, isolates belonging to lineage AA collectively harboured significantly higher genotypic and phenotypic diversity than lineage AB isolates. Together these results illustrate the important roles of reproductive modes and geographical structure in the generation and maintenance of virulence diversity in populations of M. lini .     

The division of labor: genotypic versus phenotypic specialization

A model of the division of labor in simple evolving systems is explored to compare two strategies evident in natural populations: phenotypic specialization (such as differentiation by regulated gene expression) and genotypic specialization (such as co-infection by complementary covirus populations). While genotypic specialization is vulnerable to the chance extinction of an essential specialist type and to parasitism, phenotypic specialization is able to overcome these hurdles. When simple spatial effects are included, phenotypic specialization has further benefits, protecting against destructive dynamic patterns. Many of the advantages of phenotypic specialization, however, can only be realized when a high degree of relatedness within groups is ensured.     

Biosynthesis and secretion of M- and Z-type alpha 1-proteinase inhibitor by human monocytes. Effect of inhibitors of glycosylation and of oligosaccharide processing on secretion and function

The biosynthesis and secretion of M-type and Z-type alpha 1-antitrypsin was studied in human monocytes. In monocytes of PiMM individuals alpha 1-antitrypsin represented 0.08% of the newly synthesized proteins and 0.44% of the secreted proteins. Two molecular forms of alpha 1-antitrypsin could be identified: a 51-kDa intracellular form, susceptible to endoglucosaminidase H, thus representing the high-mannose type precursor form and a 56-kDa form resistant to endoglucosaminidase H which was secreted into the medium. Inhibition of de novo glycosylation by tunicamycin impaired the secretion of M-type alpha 1-antitrypsin by about 75% whereas inhibition of oligosaccharide processing by the mannosidase II inhibitor swainsonine did not alter the secretion of M-type alpha 1-antitrypsin. alpha 1-Antitrypsin secreted by human monocytes was functionally active as measured by complex formation with porcine pancreatic elastase. Even unglycosylated alpha 1-antitrypsin secreted by human monocytes treated with tunicamycin formed a complex with elastase. In monocytes of PiZZ individuals the secretion of alpha 1-antitrypsin was decreased. 72% of newly synthesized M-type alpha 1-antitrypsin, but only 35% of newly synthesized Z-type alpha 1-antitrypsin were secreted during a labeling period of 3 h with [35S]methionine. The 51-kDa form of Z-type alpha 1-antitrypsin accumulated intracellularly, whereas the 56-kDa form was secreted. Inhibition of oligosaccharide processing by swainsonine did not alter the decreased secretion of Z-type alpha 1-antitrypsin, whereas inhibition of de novo glycosylation by tunicamycin blocked the secretion of Z-type alpha 1-antitrypsin completely.     

THE GENETIC STRUCTURE OF LARGE-LAKE DAPHNIA POPULATIONS

Cyclical parthenogenesis allows study of the genetic and evolutionary characteristics of groups exhibiting both asexual and sexual reproduction. The cladoceran genus Daphnia contains species which vary with respect to the relative incidence of sexual reproduction; pond species tend to undergo sexual reproduction more regularly than species found in large lakes. Previous genetic studies have focused on pond populations, generating expectations about large-lake populations that have not been fully met by recent studies. The present study of the Palearctic species Daphnia galeata further examines the genetic structure of large-lake populations. Nine local populations, from lakes in northern Germany, are examined for genetic variation at seven enzyme loci. Populations exhibit similar allelic arrays and often similar allele frequencies at the five polymorphic loci; values of Nei's genetic distance (D) ranged from 0.002 to 0.239, with a mean of 0.084. F_ST values range from 0.012 to 0.257, and spatial autocorrelation coefficients range from -0.533 to 0.551, for the eight alleles analyzed. With few exceptions, within-population genotypic frequencies were in Hardy-Weinberg equilibrium. There was, however, significant heterogeneity in genotypic frequencies among populations. The number of coexisting clonal groups, as determined by three locus genotypes, is high within populations. Clonal groups are widely distributed among localities. The amount of genetic divergence observed among these large-lake populations is smaller than that previously observed among pond populations and suggests that different processes may be important in determining the genetic structure and subsequent phenotypic divergence of lake versus pond populations.     

Spatial and temporal genetic variability in French populations of the peach-potato aphid,Myzus persicae

The peach-potato aphid, Myzus persicae (Sulzer), has a complex reproductive mode in which some lineages reproduce by continuous parthenogenesis, whereas others reproduce sexually once a year. The climate is thought to act directly on the reproductive mode, because sexual eggs are the only form that can resist frost in cold regions. Sexual reproduction necessitates an obligatory host alternation that may result in long-distance dispersal. Here, we examined the genetic variability at seven microsatellite loci of populations of M. persicae in France, where both reproductive modes occur. We provide clear genetic evidence that the breeding system affects genotypic variability, as cyclically parthenogenetic aphids are far more variable than their obligately parthenogenetic counterparts. A temporal decrease in genetic variability and a temporal genetic differentiation effect suggest the existence of selective factors that play an important role in shaping the genetic structure of M. persicae populations. Lastly, differences in the population structure between reproductive modes suggest that the migration associated with the change of host during sexual reproduction lowers the level of population differentiation.     

Multilocus test for introgression between the cactophilic species Drosophila mojavensis and Drosophila arizonae

Information obtained from laboratory studies regarding the efficacy of barriers to gene flow (reproductive isolation) between species is often incomplete or misleading, so detailed genetic analyses are needed to determine whether hybridization and introgression occur in nature. Previous laboratory studies of the cactophilic species Drosophila mojavensis and Drosophila arizonae suggest that reproductive isolation is incomplete and that gene flow may occur in sympatry. We sampled 18 nuclear and one mitochondrial loci from multiple populations of D. arizonae and D. mojavensis to test for the signature of recent or historic gene flow between these two species. We located chromosomal regions that were inverted between these species and analyzed those regions independently of others. Statistical tests for introgression using all loci or only collinear loci failed to reject expectations of an isolation model. Further tests using average nucleotide differences between species and phylogenetic analyses also failed to find support for introgression between D. mojavensis and D. arizonae. Additional ecological and behavioral studies of these species in their natural habitats are required to explain why the signature of gene flow was not detected at the DNA sequence level in populations when laboratory studies suggest such gene flow should be possible.     

Resilience of Zostera muelleri seagrass to small‐scale disturbances: the relative importance of asexual versus sexual recovery

Resilience is the ability of an ecosystem to recover from disturbance without loss of essential function. Seagrass ecosystems are key marine and estuarine habitats that are under threat from a variety of natural and anthropogenic disturbances. The ability of these ecosystems to recovery from disturbance will to a large extent depend on the internsity and scale of the disturbance, and the relative importance of sexual versus asexual reproduction within populations. Here, we investigated the resilience of Zostera muelleri seagrass (Syn. Zostera capricorni) to small‐scale disturbances at four locations in Lake Macquarie – Australia's largest coastal lake – and monitored recovery over a 65‐week period. Resilience of Z. muelleri varied significantly with disturbance intensity; Z. muelleri recovered rapidly (within 2 weeks) from low‐intensity disturbance (shoot loss), and rates of recovery appeared related to initial shoot length. Recovery via rhizome encroachment (asexual regeneration) from high‐intensity disturbance (loss of entire plant) varied among locations, ranging from 18‐35 weeks, whereas the ability to recover was apparently lost (at least within the time frame of this study) when recovery depended on sexual regeneration, suggesting that seeds do not provide a mechanism of recovery against intense small‐scale disturbances. The lack of sexual recruits into disturbed sites is surprising as our initial surveys of genotypic diversity (using nine polymorphic microsatellite loci) at these location indicate that populations are maintained by a mix of sexual and asexual reproduction (genotypic diversity [R] varied from 0.24 to 0.44), and populations consisted of a mosaic of genotypes with on average 3.6 unique multilocus genotypes per 300 mm diameter plot. We therefore conclude that Z. muelleri populations within Lake Macquarie rely on clonal growth to recover from small‐scale disturbances and that ongoing sexual recruitment by seeds into established seagrass beds (as opposed to bare areas arising from disturbance) must be the mechanism responsible for maintaining the observed mixed genetic composition of Z. muelleri seagrass meadows.     

Genetic Color Morphs in the Eastern Mosquitofish Experience Different Social Environments in the Wild and Laboratory

The social environment of an animal is an especially interesting component of its environment because it can be shaped by both genetic and non‐genetic variation among social partners. Indirect genetic effects (IGEs) are those created when genetic variation in social partners contributes to variation in an individual's phenotype; a potentially common form of IGE occurs when the expression of a behavioral phenotype depends on the particular genotypic combination of interacting individuals. Although IGEs can profoundly affect individual‐ and group‐level fitness, population dynamics, and even community structure, understanding their importance is complicated by two inherent challenges: (1) identifying individuals with genetic differences in social interactions that can contribute to IGEs and (2) characterizing natural social interactions that potentially involve IGEs. As a first step toward addressing both these challenges in the same system, we investigated social interactions involving genetically distinct male color morphs in the poeciliid fish Gambusia holbrooki under natural and laboratory conditions. Previous work indicates that melanic (M) and silver (S) males differ in social behavior and in how conspecifics respond to them, suggesting the potential for IGEs. We used a combination of live and video recording of social groups in two natural populations and in the laboratory to determine the potential for IGEs to contribute to behavioral variation in this species. We found that M males had more social partners, and especially more female social partners than did S males, in nature and in the laboratory. These results suggest that both direct and indirect genetic effects have the potential to play a role in the expression and evolution of social behavior in G. holbrooki.     

Enzyme Variability in Natural Populations of DAPHNIA MAGNA III. Genotypic Frequencies in Intermittent Populations

In temporary habitats populations of the cyclical parthenogen, Daphnia magna, are re-established each year from sexual eggs and reproduce parthenogenetically for two or at most three generations. The genetic effects of this breeding system have been investigated by analyzing allozyme frequencies in nineteen intermittent populations.—Genotypic frequencies at polymorphic loci were ordinarily found to be in good agreement with Hardy-Weinberg proportions and disequilibria between loci were not observed. Although significant changes in gene frequencies were observed both during and between successive cycles, there was no evidence of the marked instability of genotype frequencies characteristic of permanent populations. The recombinational degradation of genotypes at the end of each annual cycle in temporary habitats effectively prevents the genotypic structuring which develops when continued parthenogenesis is possible.     

Molecular-Marker-Facilitated Investigations of Quantitative-Trait Loci in Maize. I. Numbers, Genomic Distribution and Types of Gene Action

Individual genetic factors which underlie variation in quantitative traits of maize were investigated in each of two F2 populations by examining the mean trait expressions of genotypic classes at each of 17-20 segregating marker loci. It was demonstrated that the trait expression of marker locus classes could be interpreted in terms of genetic behavior at linked quantitative trait loci (QTLs). For each of 82 traits evaluated, QTLs were detected and located to genomic sites. The numbers of detected factors varied according to trait, with the average trait significantly influenced by almost two-thirds of the marked genomic sites. Most of the detected associations between marker loci and quantitative traits were highly significant, and could have been detected with fewer than the 1800-1900 plants evaluated in each population. The cumulative, simple effects of marker-linked regions of the genome explained between 8 and 40% of the phenotypic variation for a subset of 25 traits evaluated. Single marker loci accounted for between 0.3% and 16% of the phenotypic variation of traits. Individual plant heterozygosity, as measured by marker loci, was significantly associated with variation in many traits. The apparent types of gene action at the QTLs varied both among traits and between loci for given traits, although overdominance appeared frequently, especially for yield-related traits. The prevalence of apparent overdominance may reflect the effects of multiple QTLs within individual marker-linked regions, a situation which would tend to result in overestimation of dominance. Digenic epistasis did not appear to be important in determining the expression of the quantitative traits evaluated. Examination of the effects of marked regions on the expression of pairs of traits suggests that genomic regions vary in the direction and magnitudes of their effects on trait correlations, perhaps providing a means of selecting to dissociate some correlated traits. Marker-facilitated investigations appear to provide a powerful means of examining aspects of the genetic control of quantitative traits. Modifications of the methods employed herein will allow examination of the stability of individual gene effects in varying genetic backgrounds and environments.     

PHENOTYPIC VARIATION AND GENOTYPIC DIVERSITY IN A PLANKTONIC POPULATION OF THE TOXIGENIC MARINE DINOFLAGELLATE ALEXANDRIUM TAMARENSE (DINOPHYCEAE)1

Multiple clonal isolates from a geographic population of Alexandrium tamarense (M. Lebour) Balech from the North Sea exhibited high genotypic and phenotypic variation. Genetic heterogeneity was such that no clonal lineage was repeatedly sampled according to genotypic markers specified by amplified fragment length polymorphism (AFLP) and microsatellites. Subsampling of genotypic data from both markers showed that ordination of individuals by pair‐wise genetic dissimilarity indices was more reliable by AFLP (482 biallelic loci) than by microsatellites (18 loci). However, resulting patterns of pair‐wise genetic similarities from both markers were significantly correlated (Mantel test P < 0.005). The composition of neurotoxins associated with paralytic shellfish poisoning (PSP) was also highly diverse among these isolates and allowed clustering of toxin phenotypes based on prevalence of individual toxins. Correlation analysis of pair‐wise relatedness of individual clones according to PSP‐toxin profiles and both genotypic characters failed to yield close associations. The expression of allelochemical properties against the cryptophyte Rhodomonas salina (Wis?ouch) D. R. A. Hill et Wetherbee and the predatory dinoflagellate Oxyrrhis marina Dujard. manifested population‐wide variation of responses in the target species, from no visible effect to complete lysis of target cells. Whereas the high genotypic variation indicates high potential for adaptability of the population, we interpret the wide phenotypic variation as evidence for lack of strong selective pressure on respective phenotypic traits at the time the population was sampled. Population markers as applied here may elucidate the ecological significance of respective traits when followed under variable environmental conditions, thereby revealing how variation is maintained within populations.     

Genetic divergence and a hybrid zone between Baltic and North Sea Mytilus populations (Mytilidae: Mollusca)

Populations of the common mussel ( Mytilus edulis ) from the North Sea area (Skakerrak-Kattegat) and those from the Baltic Sea are almost diagnostically differentiated at five out of 22 studied allozyme loci; at a further seven loci, alleles predominant or common in one area are nearly absent in the other. Genetic distance was estimated at 0.28; this is similar to the distances of these populations to the Mediterranean mussel M. galloprovincialis. The three mussel types obviously represent equal evolutionary divergence from one another, and should also be taxonomically equally separated; a semispecies rank within a more comprehensive M. edulis complex or superspecies is suggested. The age of the Baltic mussel type ( 'M. trossulus' ), as an independent evolutionary lineage, is probably far greater than that of the post-glacial Baltic Sea.
Allele frequencies change gradually and in parallel when entering from the Kattegat through the Sound into the Baltic. Only a slight Wahlund effect at the strongly diverged Gpi and Pgm loci was found in intermediate populations, indicating that extensive hybridization of the two taxa takes place in the area. However, strong interlocus genotypic associations suggest that selection against hybrids is intense in later generations; the c. 100 km wide hybrid zone is narrow relative to the dispersal distance. The genotypic structure of the Lap locus does not conform with those of the other loci studied in the hybrid zone; it cannot be viewed merely as a neutral marker of the process of hybridization.     

Patterns, sources and ecological implications of clonal diversity in apomictic Ranunculus carpaticola (Ranunculus auricomus complex, Ranunculaceae)

Sources and implications of genetic diversity in agamic complexes are still under debate. Population studies (amplified fragment length polymorphisms, microsatellites) and karyological methods (Feulgen DNA image densitometry and flow cytometry) were employed for characterization of genetic diversity and ploidy levels of 10 populations of Ranunculus carpaticola in central Slovakia. Whereas two diploid populations showed high levels of genetic diversity, as expected for sexual reproduction, eight populations are hexaploid and harbour lower degrees of genotypic variation, but maintain high levels of heterozygosity at many loci, as is typical for apomicts. Polyploid populations consist either of a single AFLP genotype or of one dominant and a few deviating genotypes. genotype/genodive and character incompatibility analyses suggest that genotypic variation within apomictic populations is caused by mutations, but in one population probably also by recombination. This local facultative sexuality may have a great impact on regional genotypic diversity. Two microsatellite loci discriminated genotypes separated by the accumulation of few mutations ('clone mates') within each AFLP clone. Genetic diversity is partitioned mainly among apomictic populations and is not geographically structured, which may be due to facultative sexuality and/or multiple colonizations of sites by different clones. Habitat differentiation and a tendency to inhabit artificial meadows is more pronounced in apomictic than in sexual populations. We hypothesize that maintenance of genetic diversity and superior colonizing abilities of apomicts in temporally and spatially heterogeneous environments are important for their distributional success.     

The population genetics of clonal and partially clonal diploids

The consequences of variable rates of clonal reproduction on the population genetics of neutral markers are explored in diploid organisms within a subdivided population (island model). We use both analytical and stochastic simulation approaches. High rates of clonal reproduction will positively affect heterozygosity. As a consequence, nearly twice as many alleles per locus can be maintained and population differentiation estimated as F(ST) value is strongly decreased in purely clonal populations as compared to purely sexual ones. With increasing clonal reproduction, effective population size first slowly increases and then points toward extreme values when the reproductive system tends toward strict clonality. This reflects the fact that polymorphism is protected within individuals due to fixed heterozygosity. Contrarily, genotypic diversity smoothly decreases with increasing rates of clonal reproduction. Asexual populations thus maintain higher genetic diversity at each single locus but a lower number of different genotypes. Mixed clonal/sexual reproduction is nearly indistinguishable from strict sexual reproduction as long as the proportion of clonal reproduction is not strongly predominant for all quantities investigated, except for genotypic diversities (both at individual loci and over multiple loci).