Takuya Nakazato

Hybrid Incompatibility “Snowballs” Between Solanum Species

Rolling Snowballs The genetic incompatibilities that separate ongoing speciation events have been hypothesized by the Dobzhansky-Muller model of speciation to snowball—that is, accumulate mutations causing postzygotic isolation at a faster rate than the linear accumulation of mutations. This occurs because of potential deleterious epistatic interactions in hybrids involving two or more interacting genes. Testing QTLs (quantitative trait loci) in seed and pollen sterility between multiple species pairs in the plant group Solanum, Moyle and Nakazato (p. 1521) show that hybrid female (seed) sterility accumulates exponentially between increasingly distant species pairs, although not for hybrid male (pollen) sterility. In contrast, loci contributing to differences in other traits show no evidence for nonlinear accumulation over time. Matute et al. (p. 1518) come to similar conclusions through the use of deletion mapping in comparisons between two pairs of species of Drosophila. The number of genes causing postzygotic isolation grows as fast as the square of the number of substitutions between two species. Thus, a hybrid snowball effect is found in both plants and animals. Two studies support the theory that the number of genes involved in hybrid incompatibility increases faster than linearly. Among the reproductive barriers that can isolate species, hybrid sterility is frequently due to dysfunctional interactions between loci that accumulate between differentiating lineages. Theory describing the evolution of these incompatibilities has generated the prediction, still empirically untested, that loci underlying hybrid incompatibility should accumulate faster than linearly with time—the “snowball effect.” We evaluated the accumulation of quantitative trait loci (QTL) between species in the plant group Solanum and found evidence for a faster-than-linear accumulation of hybrid seed sterility QTL, thus empirically evaluating and confirming this theoretical prediction. In comparison, loci underlying traits unrelated to hybrid sterility show no evidence for an accelerating rate of accumulation between species.

Comparative Mapping and Rapid Karyotypic Evolution in the Genus Helianthus

Comparative genetic linkage maps provide a powerful tool for the study of karyotypic evolution. We constructed a joint SSR/RAPD genetic linkage map of the Helianthus petiolaris genome and used it, along with an integrated SSR genetic linkage map derived from four independent H. annuus mapping populations, to examine the evolution of genome structure between these two annual sunflower species. The results of this work indicate the presence of 27 colinear segments resulting from a minimum of eight translocations and three inversions. These 11 rearrangements are more than previously suspected on the basis of either cytological or genetic map-based analyses. Taken together, these rearrangements required a minimum of 20 chromosomal breakages/fusions. On the basis of estimates of the time since divergence of these two species (750,000–1,000,000 years), this translates into an estimated rate of 5.5–7.3 chromosomal rearrangements per million years of evolution, the highest rate reported for any taxonomic group to date.

ENVIRONMENTAL FACTORS PREDICT ADAPTIVE PHENOTYPIC DIFFERENTIATION WITHIN AND BETWEEN TWO WILD ANDEAN TOMATOES

Abstract Environmental variation is widely viewed as a major force driving morphological change and speciation. Although many environmental attributes are potentially critical for adaptive responses within and between species, the individual and relative importance of these diverse attributes remain poorly understood. Here we combine a geographical information systems (GIS)-based analysis of environmental variation with a multipopulation analysis of phenotypic, physiological, and genetic variation, to generate and test hypotheses of environmental factors likely driving adaptive divergence within and between two wild Andean plant species. First, we document large environmental differences between population locations of the two species, and among regions within species. Second, we show evidence for inter- and intraspecific differences in genetically based phenotypic and physiological variation. Third, combining these data, we report evidence for trait–environment associations both among populations within species, and between species, that are strongly indicative of recent and rapid adaptive responses. Finally, we show that these trait–environment associations cannot be simply explained by genetic relatedness within species, reinforcing our inference that local, regional, and species-wide environmental conditions are responsible for phenotypic and physiological diversification. The strongest trait–environment associations involve temperature and precipitation gradients, suggesting these climatic factors are predominant drivers of adaptive diversification in these species.

Comparative Genetics of Hybrid Incompatibility: Sterility in Two Solanum Species Crosses

The genetic basis of hybrid sterility can provide insight into the genetic and evolutionary origins of species barriers. We examine the genetics of hybrid incompatibility between two diploid plant species in the plant clade Solanum sect. Lycopersicon. Using a set of near-isogenic lines (NILs) representing the wild species Solanum pennellii (formerly Lycopersicon pennellii) in the genetic background of the cultivated tomato S. lycopersicum (formerly L. esculentum), we found that hybrid pollen and seed infertility are each based on a modest number of loci, male (pollen) and other (seed) incompatibility factors are roughly comparable in number, and seed-infertility QTL act additively or recessively. These findings are remarkably consistent with our previous analysis in a different species pair, S. lycopersicum × S. habrochaites. Data from both studies contrast strongly with data from Drosophila. Finally, QTL for pollen and seed sterility from the two Solanum studies were chromosomally colocalized, indicating a shared evolutionary history for these QTL, a nonrandom genomic distribution of loci causing sterility, and/or a proclivity of certain genes to be involved in hybrid sterility. We show that comparative mapping data can delimit the probable timing of evolution of detected QTL and discern which sterility loci likely evolved earliest among species.

Genetic Map-Based Analysis of Genome Structure in the Homosporous Fern Ceratopteris richardii

Homosporous ferns have extremely high chromosome numbers relative to flowering plants, but the species with the lowest chromosome numbers show gene expression patterns typical of diploid organisms, suggesting that they may be diploidized ancient polyploids. To investigate the role of polyploidy in fern genome evolution, and to provide permanent genetic resources for this neglected group, we constructed a high-resolution genetic linkage map of the homosporous fern model species, Ceratopteris richardii (n = 39). Linkage map construction employed 488 doubled haploid lines (DHLs) that were genotyped for 368 RFLP, 358 AFLP, and 3 isozyme markers. Forty-one linkage groups were recovered, with average spacing between markers of 3.18 cM. Most loci (∼76%) are duplicated and most duplicates occur on different linkage groups, indicating that as in other eukaryotic genomes, gene duplication plays a prominent role in shaping the architecture of fern genomes. Although past polyploidization is a potential mechanism for the observed abundance of gene duplicates, a wide range in the number of gene duplicates as well as the absence of large syntenic regions consisting of duplicated gene copies implies that small-scale duplications may be the primary mode of gene duplication in C. richardii. Alternatively, evidence of past polyploidization(s) may be masked by extensive chromosomal rearrangements as well as smaller-scale duplications and deletions following polyploidization(s).

Complex Epistasis for Dobzhansky–Muller Hybrid Incompatibility in Solanum

We examined the prevalence of interactions between pairs of short chromosomal regions from one species (Solanum habrochaites) co-introgressed into a heterospecific genetic background (Solanum lycopersicum). Of 105 double introgression line (DIL) families generated from a complete diallele combination of 15 chromosomal segments, 39 (∼38%) showed evidence for complex epistasis in the form of genotypic and/or allelic marker transmission distortion in DIL F2 populations.

Biology and Evolution of Ferns and Lycophytes: Evolution of the nuclear genome of ferns and lycophytes

Introduction Analyses of gene expression and function, genetic networks, population polymorphisms, and genome organization at the whole genome level have enabled research on previously intractable questions (reviewed in Wolfe and Li, 2003). Among plant lineages, genomic approaches have been most widely applied in the angiosperms, where significant resources have been developed. Angiosperm studies utilizing genome scale analyses have made several important advances, including the identification of an extensive history of genome duplications (Blanc et al ., 2003; Schlueter et al ., 2004; Cui et al ., 2006), progress in understanding flower development and evolution (Doust et al ., 2005; Whibley et al ., 2006), characterization of the genetics underlying speciation and adaptation (Bradshaw and Schemske, 2003; Rieseberg et al ., 2003; Lai et al ., 2005; Eyre-Walker, 2006), the identification and mapping of recombination hot spots (Drouaud et al ., 2006), and the discovery and role of microRNAs (Bartel and Bartel, 2003; Bartel, 2004). Genomic analyses will undoubtedly continue to provide tests of longstanding questions and offer novel perspectives in biology. For example, modern genomic analyses are capable of explaining the origin of the exceptionally high chromosome numbers of homosporous ferns and lycophytes, a result that will shed light on eukaryotic genome organization and evolution. Although there are rich biological and taxonomic resources for ferns and lycophytes, the genomics of these seed-free plants is still in its infancy, and the tools necessary for genomic studies lag behind those available for seed plants. The first homosporous fern linkage map was published only recently (Nakazato et al ., 2006), whereas a large number of linkage maps for seed plants have accumulated since the 1980s

A genomewide study of reproductive barriers between allopatric populations of a homosporous fern, Ceratopteris richardii.

Biological factors involved in reproductive barriers between two divergent races of Ceratopteris richardii were investigated. We used a combination of spore germination rates, QTL analysis of spore germination rates, and transmission ratio distortion (TRD) of 729 RFLPs, AFLPs, and isozyme markers distributed across the genome on the basis of hybrid populations of 488 doubled haploid lines (DHLs) and 168 F2s. Substantial reproductive barriers were found between the parental races, predominantly in the form of spore inviability (23.7% F1 spore viability). Intrinsic genetic factors such as Bateson–Dobzhansky–Muller (BDM) incompatibilities involving both nuclear–nuclear and nuclear–cytoplasmic factors and chromosomal rearrangements appear to contribute to intrinsic postzygotic isolation. The genomewide distribution patterns of TRD loci support the hypothesis that reproductive barriers are a byproduct of divergence in allopatry and that the strong reproductive barriers are attributable to a small number of genetic elements scattered throughout the genome.

The genetic basis of speciation in the Giliopsis lineage of Ipomopsis(Polemoniaceae)

One of the most powerful drivers of speciation in plants is pollinator-mediated disruptive selection, which leads to the divergence of floral traits adapted to the morphology and behavior of different pollinators. Despite the widespread importance of this speciation mechanism, its genetic basis has been explored in only a few groups. Here, we characterize the genetic basis of pollinator-mediated divergence of two species in genus Ipomopsis, I. guttata and I. tenuifolia, using quantitative trait locus (QTL) analyses of floral traits and other variable phenotypes. We detected one to six QTLs per trait, with each QTL generally explaining small to modest amounts of the phenotypic variance of a backcross hybrid population. In contrast, flowering time and anthocyanin abundance (a metric of color variation) were controlled by a few QTLs of relatively large effect. QTLs were strongly clustered within linkage groups, with 26 of 37 QTLs localized to six marker-interval ‘hotspots,’ all of which harbored pleiotropic QTLs. In contrast to other studies that have examined the genetic basis of pollinator shifts, our results indicate that, in general, mutations of small to modest effect on phenotype were involved. Thus, the evolutionary transition between the distinct pollination modes of I. guttata and I. tenuifolia likely proceeded incrementally, rather than saltationally.

Spatial genetics of wild tomato species reveals roles of the Andean geography on demographic history

PREMISE OF THE STUDY Understanding the demographic history of natural populations in relation to the geographic features in their habitats is an important step toward deciphering the mechanisms of evolutionary processes in nature. This study investigates how the complex geographic and ecological features of the Andes play a role in demographic history, species divergence, dispersal patterns, and hybridization in wild tomato species. METHODS We investigated spatial genetics of two closely related wild tomato species, Solanum lycopersicum and S. pimpinellifolium, by integrating amplified fragment length polymorphism (AFLP) marker data and geographic information system (GIS)-derived geographic and climatic data. KEY RESULTS The two species represent genetically distinct lineages largely separated by the Andes, but hybridize extensively in central to northern Ecuador, likely mediated by the transitional climatic conditions between those of the two species. Solanum lycospericum has likely experienced a severe population bottleneck during the colonization of the eastern Andes followed by a rapid population expansion. CONCLUSIONS The study demonstrates that the evolutionary patterns of the two wild tomatoes, including demographic history, dispersal patterns, interspecific divergence, and hybridization, are intimately related to the complex geographic and ecological features of the Andes. Integrating genetic data across the genome and GIS-derived environmental data can provide insights into the patterns of complex evolutionary processes in nature.