Robert G. Latta

Adaptive population divergence: markers, QTL and traits

Abstract Molecular markers appear to be poor indicators of heritable variation in adaptive traits. Direct comparison of population structure in markers with that in traits is made possible by the measure Q st , which partitions quantitative genetic variation in a manner analogous to F st for single gene markers. A survey of the literature reveals that mean Q st is typically larger than and poorly correlated with mean F st across 29 species. Within species, Q st varies widely among traits; traits experiencing the strongest local selection pressures are expected to be the most divergent from molecular F st . Thus, Q st will be particularly relevant to conservation efforts where preserving extant adaptation to local environments is an important goal. Recent theoretical and simulation studies suggest however that F st is a better predictor of the pattern of allelic differentiation at quantitative trait loci (QTLs) than is Q st in random mating populations, in which case allelic variation at QTLs might be better assessed by molecular markers than will extant variation in the traits themselves.

Differentiation of Allelic Frequencies at Quantitative Trait Loci Affecting Locally Adaptive Traits

σ 2 t 5 (1 1 Fst)σ 0 , Direct comparisons of population differentiation obwhere σ w, σ b, and σ t are the within-population, beserved in neutral loci with that seen in quantitative traits tween-population, and total genetic variances in the trait, have revealed discordant patterns, most commonly that respectively, and σ 0 is the genetic variance for the trait quantitative traits are more differentiated than single expected if the populations formed a single panmictic neutral loci. For example, body size has a greater prounit (Wright 1951, 1952; Lande 1992). Thus an estimate portion of genetic variation attributable to amongof population differentiation for quantitative traits population differences than do presumed neutral allo(termed Qst by Spitze 1993) can be computed as zymes in both Drosophila buzzatii (Prout and Barker

DIRECT AND INDIRECT ESTIMATES OF SEED VERSUS POLLEN MOVEMENT WITHIN A POPULATION OF PONDEROSA PINE

We examined the spatial distribution of maternally inherited mitochondrial DNA and paternally inherited chloroplast DNA polymorphisms in a permanently marked stand of ponderosa pine (Pinus ponderosa Laws). Movement of maternally inherited mtDNA occurs only via seed dispersal, and mtDNA haplotypes showed significant patch structure. Moreover, individuals within patches identified by mtDNA haplotypes were related approximately as half‐sibs based upon analysis of allozyme genotypes. Thus, seed dispersal is limited within the population, and creates matrilineal clusters in space. By contrast, paternally inherited cpDNA is dispersed by movement of both seed and pollen. Chloroplast DNA polymorphisms showed no evidence of patch structure, but rather a weak (and nonsignificant) trend toward hyperdispersion, suggesting nearly unlimited movement of pollen among trees within this stand. Two of the trees had unique allozyme alleles, which were used to directly measure pollen movement away from those trees. Marked pollen was as likely to disperse across the population as it was to fertilize near neighbors.

FITNESS CONSEQUENCES OF HYBRIDIZATION BETWEEN ECOTYPES OF AVENA BARBATA: HYBRID BREAKDOWN, HYBRID VIGOR, AND TRANSGRESSIVE SEGREGATION

Abstract Hybridization is an important factor in the evolution of plants; however, many of the studies that have examined hybrid fitness have been concerned with the study of early generation hybrids. We examined the early- and late-generation fitness consequences of hybridization between two ecotypes of the selfing annual Avena barbata in a greenhouse environment as well as in two natural environments. Fitness of early generation (F2) hybrids reflects both the action of dominance effects (hybrid vigor) and recombination (hybrid breakdown) and was not significantly different from that of the midparent in any environment. Fitness of later generation (F6) recombinant inbred lines (RILS) derived from the cross reflect both the loss of early generation heterozygosity as well as disruption of any coadapted gene complexes present in the parents. In all environments, F6 RILs were on average significantly less fit than the (equally homozygous) midparent, indicating hybrid breakdown through the disruption of epistatic interactions. However, the inbred F6 were also less fit than the heterozygous F2, indicating that hybrid vigor also occurs in A. barbata, and counteracts hybrid breakdown in early generation hybrids. Also, although the F6 generation mean is lower than the midparent mean, there are individual genotypes within the F6 generation that are capable of outperforming the parental ecotypes in the greenhouse. Fewer hybrid genotypes are capable of outperforming the parental ecotypes in the field. Overall, these experiments demonstrate how a single hybridization event can result in a number of outcomes including hybrid vigor, hybrid breakdown, and transgressive segregation, which interact to determine long-term hybrid fitness.

Glacial refugia of limber pine (Pinus flexilis James) inferred from the population structure of mitochondrial DNA

To make inferences about the glacial refugia that harboured the limber pine, Pinus flexilis James, we examined the range‐wide population structure of mitochondrial DNA (mtDNA) with eight size variants in the second intron of nad1. The data consisted of haplotypes from 704 trees collected from 40 localities. The value of FST for these populations was 0.80, which is a much larger value than has been reported for allozymes and chloroplast DNA (cpDNA) in limber pine, and it suggests that the number of seeds moving among localities per generation is ≈ 0.12. Gene flow of this magnitude would allow mutation and subsequent genetic drift to have a substantial impact on the population structure of mtDNA. The majority of the mtDNA haplotypes are restricted to minor portions of the geographical range. The data are consistent with mtDNA differentiation in seven glacial refugia, followed by dispersal out of those refugia.

The relationship between inbreeding depression and prior inbreeding among populations of four Mimulus taxa

When recessive mutations are the primary cause of inbreeding depression, a negative relationship between the levels of prior inbreeding and inbreeding depression is expected. We tested this prediction using 15 populations chosen a priori to represent a wide range of prior inbreeding among four closely related taxa of the Mimulus guttatus species complex. Artificially selfed and outcrossed progeny were grown under controlled growth‐chamber conditions, and inbreeding depression was estimated for each population as one minus the ratio of the fitness of selfed to outcrossed progeny. Estimates of inbreeding depression varied from 0% to 68% among populations. Inbreeding coefficients, estimated from electrophoretic assay of field‐collected progenies, ranged from 0.02 to 0.76. All five fitness traits displayed a negative association between inbreeding depression and the inbreeding coefficient, but only height showed a statistically significant correlation. Inbreeding depression was also not correlated with the level of genetic variability. In addition, populations with similar levels of prior inbreeding showed significant differences of inbreeding depression, whereas populations with different levels of prior inbreeding showed similar inbreeding depression. Within populations, inbreeding depression did not differ between progeny selfed one versus two generations. Our results are weakly consistent with the recessive mutation model of inbreeding depression, but suggest that additional factors, including genotype‐by‐environment interaction and complex modes of inheritance, may influence the expression of inbreeding depression.

Identifying loci under selection across contrasting environments in Avena barbata using quantitative trait locus mapping.

We constructed recombinant inbred lines of a cross between naturally occurring ecotypes of Avena barbata (Pott ex Link), Poaceae, associated with contrasting moisture environments. These lines were assessed for fitness in common garden reciprocal transplant experiments in two contrasting field sites in each of two years, as well as a novel, benign greenhouse environment. An AFLP (amplified fragment length polymorphism) linkage map of 129 markers spanned 644 cM in 19 linkage groups, which is smaller, with more linkage groups, than expected. Therefore parts of the A. barbata genome remain unmapped, possibly because they lack variation between the ecotypes. Nevertheless, we identified QTL (quantitative trait loci) under selection in both native environments and in the greenhouse. Across years at the same site, the same loci remain under selection, for the same alleles. Across sites, an overlapping set of loci are under selection with either (i) the same alleles favoured at both sites or (ii) loci under selection at one site and neutral at the other. QTL under selection in the greenhouse were generally unlinked to those under selection in the field because selection acted on a different trait. We found little evidence that selection favours alternate alleles in alternate environments, which would be necessary if genotype by environment interaction were to maintain genetic variation in A. barbata. Additive effect QTL were best able to explain the genetic variation among recombinant inbred lines for the greenhouse environment where heritability was highest, and past selection had not eliminated variation.

Shared quantitative trait loci underlying the genetic correlation between continuous traits

We review genetic correlations among quantitative traits in light of their underlying quantitative trait loci (QTL). We derive an expectation of genetic correlation from the effects of underlying loci and test whether published genetic correlations can be explained by the QTL underlying the traits. While genetically correlated traits shared more QTL (33%) on average than uncorrelated traits (11%), the actual number of shared QTL shared was small. QTL usually predicted the sign of the correlation with good accuracy, but the quantitative prediction was poor. Approximately 25% of trait pairs in the data set had at least one QTL with antagonistic effects. Yet a significant minority (20%) of such trait pairs have net positive genetic correlations due to such antagonistic QTL ‘hidden’ within positive genetic correlations. We review the evidence on whether shared QTL represent single pleiotropic loci or closely linked monotropic genes, and argue that strict pleiotropy can be viewed as one end of a continuum of recombination rates where r = 0. QTL studies of genetic correlation will likely be insufficient to predict evolutionary trajectories over long time spans in large panmictic populations, but will provide important insights into the trade‐offs involved in population and species divergence.

Mitochondrial haplotype distribution, seed dispersal and patterns of postglacial expansion of ponderosa pine

Maternally inherited mtDNA in a secondary contact zone of ponderosa pine revealed a cline less than 10 km wide — much narrower than previously described. A survey of 76 populations gave no evidence either of intermixing or of a mosaic contact zone. Such sharp contact zones are consistent with diffusive range expansion, rather than long distance colonization. However, evidence for long distance seed dispersal events was found in two populations where haplotypes were observed far from their main area of occurrence. The results suggest a small number of long distance colonists with diffusive dispersal from these centres.

Hybridization, recombination, and the genetic basis of fitness variation across environments in Avena barbata

We created Recombinant Inbred Lines (RILs) derived from a cross between ecotypes of Avena barbata associated with moist (mesic) and dry (xeric) habitats in California. Traits which were correlated with fitness across RILs mapped to the same Quantitative Trait Loci (QTLs) as fitness. However, different QTL affected fitness in different environments so that fitness was weakly correlated across environments. Recombination released considerable heritable variation both in fitness, and in ecologically relevant traits. Many traits showed transgressive segregation caused by recombination of QTL associated in repulsion phase in the parents. In addition, some traits were uncorrelated, allowing novel combinations of those traits to be created. Recombination also created heritable variation in reaction norms for at least one trait (root allocation). Altogether these results suggest that recombination can combine the most selectively advantageous genes and traits of the parents to produce broadly adapted genotypes that are capable of outperforming the parents. Indeed, two of the RILs showed higher fitness than the parental ecotypes across a range of environmental treatments in the greenhouse, but their superiority was less pronounced in the field. Although late-generation recombinants exhibited hybrid breakdown, being less fit, on average, than the mid-parent, early generation hybrids appear to exhibit hybrid vigour through the expression of dominance effects in the heterozyotes. This vigour may offset the effects of hybrid breakdown in the early generations following a cross, enhancing the opportunity for recombination to create broadly adapted genotypes. We discuss the implications of these findings to the evolution of colonizing species.