Regional differences in the abiotic environment contribute to genomic divergence within a wild tomato species.

The wild currant tomato Solanum pimpinellifolium inhabits a wide range of abiotic habitats across its native range of Ecuador and Peru. Although it has served as a key genetic resource for the improvement of domestic cultivars, little is known about the genetic basis of traits underlying local adaptation in this species, nor what abiotic variables are most important for driving differentiation. Here we use redundancy analysis (RDA) and other multivariate statistical methods (structural equation modelling [SEM] and generalized dissimilarity modelling [GDM]) to quantify the relationship of genomic variation (6,830 single nucleotide polymorphisms [SNPs]) with climate and geography, among 140 wild accessions. RDA, SEM and GDM each identified environment as explaining more genomic variation than geography, suggesting that local adaptation to heterogeneous abiotic habitats may be an important source of genetic diversity in this species. Environmental factors describing temporal variation in precipitation and evaporative demand explained the most SNP variation among accessions, indicating that these forces may represent key selective agents. Lastly, by studying how SNP-environment associations vary throughout the genome (44,064 SNPs), we mapped the location and investigated the functions of loci putatively contributing to climatic adaptations. Together, our findings indicate an important role for selection imposed by the abiotic environment in driving genomic differentiation between populations.

Genome-wide genotyping estimates mating system parameters and paternity in the island species Tolpis succulenta.

PREMISE: The mating system has profound consequences, not only for ecology and evolution, but also for the conservation of threatened or endangered species. Unfortunately, small populations are difficult to study owing to limits on sample size and genetic marker diversity. Here, we estimated mating system parameters in three small populations of an island plant using genomic genotyping. Although self-incompatible (SI) species are known to often set some self-seed, little is known about how "leaky SI" affects selfing rates in nature or the role that multiple paternity plays in small populations. METHODS: We generalized the BORICE mating system program to determine the siring pattern within maternal families. We applied this algorithm to maternal families from three populations of Tolpis succulenta from Madeira Island and genotyped the progeny using RADseq. We applied BORICE to estimate each individual offspring as outcrossed or selfed, the paternity of each outcrossed offspring, and the level of inbreeding of each maternal plant. RESULTS: Despite a functional self-incompatibility system, these data establish T. succulenta as a pseudo-self-compatible (PSC) species. Two of 75 offspring were strongly indicated as products of self-fertilization. Despite selfing, all adult maternal plants were fully outbred. There was high differentiation among and low variation within populations, consistent with a history of genetic isolation of these small populations. There were generally multiple sires per maternal family. Twenty-two percent of sib contrasts (between outcrossed offspring within maternal families) shared the same sire. CONCLUSIONS: Genome-wide genotyping, combined with appropriate analytical methods, enables estimation of mating system and multiple paternity in small populations. These data address questions about the evolution of reproductive traits and the conservation of threatened populations.

Intraspecific Genetic Variation Underlying Postmating Reproductive Barriers between Species in the Wild Tomato Clade (Solanum sect. Lycopersicon).

A goal of speciation genetics is to understand how the genetic components underlying interspecific reproductive barriers originate within species. Unilateral incompatibility (UI) is a postmating prezygotic barrier in which pollen rejection in the female reproductive tract (style) occurs in only one direction of an interspecific cross. Natural variation in the strength of UI has been observed among populations within species in the wild tomato clade. In some cases, molecular loci underlying self-incompatibility (SI) are associated with this variation in UI, but the mechanistic connection between these intra- and inter-specific pollen rejection behaviors is poorly understood in most instances. We generated an F2 population between SI and SC genotypes of a single species, Solanum pennellii, to examine the genetic basis of intraspecific variation in UI against other species, and to determine whether loci underlying SI are genetically associated with this variation. We found that F2 individuals vary in the rate at which UI rejection occurs. One large effect QTL detected for this trait co-localized with the SI-determining S-locus. Moreover, individuals that expressed S-RNase-the S-locus protein involved in SI pollen rejection-in their styles had much more rapid UI responses compared with those without S-RNase protein. Our analysis shows that intraspecific variation at mate choice loci-in this case at loci that prevent self-fertilization-can contribute to variation in the expression of interspecific isolation, including postmating prezygotic barriers. Understanding the nature of such intraspecific variation can provide insight into the accumulation of these barriers between diverging lineages.

A simple genetic architecture and low constraint allow rapid floral evolution in a diverse and recently radiating plant genus.

Genetic correlations among different components of phenotypes, especially those resulting from pleiotropy, can constrain or facilitate trait evolution. These factors could especially influence the evolution of traits that are functionally integrated, such as those comprising the flower. Indeed, pleiotropy is proposed as a main driver of repeated convergent trait transitions, including the evolution of phenotypically similar pollinator syndromes. We assessed the role of pleiotropy in the differentiation of floral and other reproductive traits between two species - Jaltomata sinuosa and J. umbellata (Solanaceae) - that have divergent suites of floral traits consistent with bee and hummingbird pollination, respectively. To do so, we generated a hybrid population and examined the genetic architecture (trait segregation and quantitative trait locus (QTL) distribution) underlying 25 floral and fertility traits. We found that most floral traits had a relatively simple genetic basis (few, predominantly additive, QTLs of moderate to large effect), as well as little evidence of antagonistic pleiotropy (few trait correlations and QTL colocalization, particularly between traits of different classes). However, we did detect a potential case of adaptive pleiotropy among floral size and nectar traits. These mechanisms may have facilitated the rapid floral trait evolution observed within Jaltomata, and may be a common component of rapid phenotypic change more broadly.

Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species.

Elevated rates of evolution in reproductive proteins are commonly observed in animal species, and are thought to be driven by the action of sexual selection and sexual conflict acting specifically on reproductive traits. Whether similar patterns are broadly observed in other biological groups is equivocal. Here, we examine patterns of protein divergence among wild tomato species (Solanum section Lycopersicon), to understand forces shaping the evolution of reproductive genes in this diverse, rapidly evolving plant clade. By comparing rates of molecular evolution among loci expressed in reproductive and non-reproductive tissues, our aims were to test if: (a) reproductive-specific loci evolve more rapidly, on average, than non-reproductive loci; (b) 'male'-specific loci evolve at different rates than 'female'-specific loci; (c) genes expressed exclusively in gametophytic (haploid) tissue evolve differently from genes expressed in sporophytic (diploid) tissue or in both tissue types; and (d) mating system variation (a potential proxy for the expected strength of sexual selection and/or sexual conflict) affects patterns of protein evolution. We observed elevated evolutionary rates in reproductive proteins. However, this pattern was most evident for female- rather than male-specific loci, both broadly and for individual loci inferred to be positively selected. These elevated rates might be facilitated by greater tissue-specificity of reproductive proteins, as faster rates were also associated with more narrow expression domains. In contrast, we found little evidence that evolutionary rates are consistently different in loci experiencing haploid selection (gametophytic-exclusive loci), or in lineages with quantitatively different mating systems. Overall while reproductive protein evolution is generally elevated in this diverse plant group, some specific patterns of evolution are more complex than those reported in other (largely animal) systems, and include a more prominent role for female-specific loci among adaptively evolving genes.

The potential role of hybridization in diversification and speciation in an insular plant lineage: insights from synthetic interspecific hybrids.

Hybridization is recognized as an important process in plant evolution, and this may be particularly true for island plants where several biotic and abiotic factors facilitate interspecific hybridization. Although rarely done, experimental studies could provide insights into the potential of natural hybridization to generate diversity when species come into contact in the dynamic island setting. The potential of hybridization to generate morphological variation was analysed within and among 12 families (inbred lines) of an F4 hybrid generation between two species of Tolpis endemic to the Canary Islands. Combinations of characters not seen in the parents were present in hybrids. Several floral and vegetative characters were transgressive relative to their parents. Morphometric studies of floral, vegetative and fruit characters revealed that several F4 families were phenotypically distinct from other families, and from their parents. The study demonstrates that morphologically distinct pollen-fertile lines, potentially worthy of taxonomic recognition if occurring in nature, can be generated in four generations. The ability of the hybrid lines to set self-seed would reduce gene flow among the lines, and among the hybrids and their parental species. Selfing would also facilitate the fixation of characters within each of the lines. Overall, the results show the considerable potential of hybridization for generating diversity and distinct phenotypes in island lineages.