Population differentiation and outbreeding depression

Etterson, J. R., S. R. Keller, and L. F. Galloway. 2007. Epistatic and cytonuclear interactions govern hybrid breakdown in the autotetraploid Campanulastrum americanum. Evolution 61: 2671-1683. (pdf reprint)
Abstract.– The consequences of combining divergent genomes among populations of a diploid species often involve F1 hybrid vigor followed by hybrid breakdown in later recombinant generations. However, as many as 70% of plant species are thought to have polyploid origins; yet little is known about the genetic architecture of divergence in polyploids and how it may differ from diploid species. We investigated the genetic architecture of population divergence using controlled crosses among five populations of the autotetraploid herb, Campanulastrum americanum . Plants were reciprocally hybridized to produce F1, F2, and F1-backcross generations that were grown with parental types in a greenhouse and measured for performance. In contrast to diploid expectations, most F1 hybrids lacked heterosis and instead showed strong outbreeding depression for early life traits. Recombinant hybrid generations often showed a recovery of performance to levels approximating, or at times even exceeding, the parental values. This pattern was also evident for an index of cumulative fitness. Analyses of line means indicated non-additive gene action, especially forms of digenic epistasis, often influenced hybrid performance. However, standard diploid genetic models were not adequate at describing the underlying genetic architecture in a number of cases. Differences between reciprocal hybrids indicated that cytoplasmic and/or cytonuclear interactions also contributed to divergence. An enhanced role of epistasis in population differentiation may be the norm in polyploids, which have more gene copies. This study, the first of its kind on a natural autotetraploid, suggests that gene duplication may cause polyploid populations to diverge in a fundamentally different way than diploids.

Galloway, L. F. and J. R. Etterson. 2005. Population differentiation and hybrid success in Campanula americana : geography and genome size. Journal of Evolutionary Biology 18: 81-89. (pdf reprint)
Abstract. – Populations within a species may diverge through genetic drift and natural selection. Few studies report on population differentiation in autopolyploids where multiple gene copies and the ratio of cytoplasmic to nuclear genes differ from diploids and may influence divergence. In autotetraploid Campanula americana we created hybrids between populations that differed in geographic proximity and genome size. Differences in genome size (up to 6.5%) did not influence hybrid performance. In contrast, hybrid performance was strongly influenced by population proximity. F1 hybrids between distant populations performed poorly relative to their parents while hybrids between proximate populations outperformed their parents. Outbreeding depression was strongest for juvenile traits. The expression of outbreeding depression often differed between reciprocal hybrids indicating interactions between nuclear and cytoplasmic genes contribute to population differentiation. Because plants were grown under greenhouse conditions, the outbreeding depression was likely due to genetic (underdominance or loss of additive-by-additive epistasis) rather than ecological factors.

Galloway, L. F. and C. B. Fenster. 2001. Nuclear and cytoplasmic contributions to intraspecific divergence in an annual legume. Evolution 55:488-497. (pdf reprint)
Abstract. – The genetic architecture of trait differentiation was evaluated between two ecologically distinct populations of Chamaecrista fasciculata. Individuals from Maryland and Illinois U.S.A. populations were crossed to create 10 types of seed: Maryland and Illinois parents, reciprocal F1 and F2 hybrids, and backcrosses to Maryland and to Illinois on reciprocal F1 hybrids. Reciprocal crosses created hybrid generation seeds with both Maryland and Illinois cytoplasmic backgrounds. Experimental individuals were grown in a common garden near the site of the Maryland population. In the garden, plants from the Illinois population flowered, set fruit, and died earlier than those from Maryland, likely reflecting adaptations to differences in growing season length between the two populations. Although reproductive components at the flower and whole plant level differed between the two populations, reproductive output as measured by fruit and seed production was similar. Cytoplasmic genes had a subtle but pervasive effect on population differentiation; hybrids with Maryland cytoplasm were significantly differentiated from those with Illinois cytoplasm when all characters were evaluated jointly. The nuclear genetic architecture of population differentiation was evaluated with joint scaling tests. Depending on the trait, both additive and nonadditive genetic effects contributed to population differentiation. Intraspecific genetic differentiation in this wild plant species appears to reflect a complex genetic architecture that includes the contribution of additive, dominance and epistatic components in addition to subtle cytoplasmic effects.

Galloway, L. F. and C. B. Fenster. 2000. Population differentiation in an annual legume: local adaptation. Evolution 54:1173-1181. (pdf reprint)
Abstract. – Studies of many plants species have demonstrated adaptive genetic differentiation to local environmental conditions. Typically these studies are conducted to evaluate adaptation to contrasting environments. As a consequence, although local adaptation has been frequently demonstrated, we have little information as to the spatial scale of adaptive evolution. We evaluated adaptive differentiation between populations of the annual legume Chamaecrista fasciculata using a replicated "common garden" design. Study sites were established in three field locations home to native populations of C. fasciculata. Each location was planted for two years with seed from the population native to the study site (home population) and populations located 6 distances (0.1-2000 km) from each site (transplanted populations). Seeds were planted into the study sites with minimum disturbance in order to determine the scale of local adaptation, as measured by a home-site fitness advantage, for five fitness components: germination, survival, vegetative biomass, fruit production, and the number of fruit produced per seed planted (an estimate of cumulative fitness). For all characters there was little evidence for local adaptation except at the furthest spatial scales. However there was genetic differentiation among some shorter distance transplants. Patterns of adaptive differentiation were fairly consistent in two of the three sites but varied between years. Little genetic variation was expressed at the third site. These results, combined with previous estimates of limited gene flow, suggest that metapopulation processes and temporal environmental variation act together, reducing local adaptation except over long distances.

Fenster, C. B. and L. F. Galloway. 2000. Population differentiation in an annual legume: genetic architecture. Evolution 54:1157-1172. (pdf reprint)
Abstract. – The presence or absence of epistasis, or gene interaction, is explicitly assumed in many evolutionary models. While many empirical studies have documented a role of epistasis in population divergence under laboratory conditions, there have been very few attempts at quantifying epistasis in the native environment where natural selection is expected to act.  In addition, we have little understanding of the frequency with which epistasis contributes to the evolution of natural populations. In this study we used a quantitative genetic design to quantify the contribution of epistasis to population divergence for fitness components of a native annual legume, Chamaecrista fasciculata. The design incorporated the contrast of performance of F2 and F3 segregating progeny of 18 interpopulation crosses with the F1 and their parents. Crosses were conducted between populations from 100 m to 2000 km apart. All generations were grown for two seasons in the natural environment of one of the parents. The F1 often outperformed the parents. This F1 heterosis reveals population structure and suggests drift is a major contributor to population differentiation. The F2 generation demonstrated that combining genes from different populations can sometimes have unexpected positive effects. However, the F3 performance indicated that combining genes from different populations decreased vigor beyond that due to the expected loss of heterozygosity. Combined with previous data, our results suggest that both selection and drift contribute to population differentiation which is based on epistatic genetic divergence. Because only the F3 consistently expressed hybrid breakdown, we conclude that the epistasis documented in our study reflects interactions among linked loci.

Fenster, C. B. and L. F. Galloway. 2000. Inbreeding and outbreeding depression in natural populations of Chamaecrista fasciculata (Fabaceae): consequences for conservation biology. Conservation Biology 14:1406-1412. (pdf reprint)
Abstract. – The deleterious consequences of inbreeding have been well documented. However, there are few empirical studies which have examined the consequences of restoring heterozygosity and hence the fitness of inbred populations by conducting interpopulation crosses and measuring the performance of later generation hybrids under field conditions. Here we conducted interpopulation crosses of 100 m - 2000 km, which spans the range of Chamaecrista fasciculata (Fabaceae) in eastern N. America. We then contrasted the performance of the F1 and later segregating F3 hybrids with the parental generation. We found almost universal F1 superiority over the parents. The F3 suffered a loss of fitness compared to the F1. The drop-off in fitness of the F3 reflects both the loss of heterozygosity as well as the disruption of coadapted gene complexes. However, the F3 performance was still often equal to that of the parents, suggesting that heterosis can out-weigh the loss of coadaptation except for the longest distance crosses. In a subset of environments the F3 performance of long distance, >1000 km interpopulation crosses, was less than both parents, and indicated true outbreeding depression. For C. fasciculata, it appears that crossing populations of up to intermediate distances of 100ís km has a short-term beneficial effect on progeny performance through the F1, and that longer-term effects are not necessarily disruptive of fitness, at least relative to parental performance.

Galloway, L. F. and C. B. Fenster. 1999. The effect of nuclear and cytoplasmic genes on fitness and local adaptation in an annual legume. Evolution 53:1734-1743. (pdf reprint)
Abstract. – The role of nuclear genes to local adaptation has been well documented. However, the role of maternally inherited cytoplasmic genes to the evolution of natural populations has been relatively unstudied. To evaluate the contribution of cytoplasmic and nuclear genomes and their interactions to local adaptation we created second generation backcross hybrids between a Maryland and an Illinois population of the annual legume Chamaecrista fasciculata.  Backcross progeny were planted in the sites native to each population for two years where we quantified germination, survivorship, fruit production, vegetative biomass and cumulative fitness.  We found limited evidence for the contribution of either cytoplasmic or nuclear genes to local adaptation.  In Maryland, plants had greater survivorship, biomass, fruit production and cumulative fitness if their nuclear genome was composed predominately of native Maryland genes; cytoplasmic genes did not affect fitness.  In Illinois, local cytoplasm marginally enhanced fitness while Maryland nuclear genes outperformed local nuclear genes.  Interactions between cytoplasmic and nuclear genes influenced seed weight, vegetative biomass and fitness, and therefore may affect evolution of these characters.  Genetic effects were stronger acting through seed size than directly on characters.  However seed size differences between the two populations were largely genetic and therefore selection on fitness components is likely to result in evolutionary change.  The contribution of nuclear and cytoplasmic genes to fitness components varied across sites and years suggesting that experiments should be replicated and conducted under natural conditions to understand the influence of these genomes and their interactions to population differentiation.

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