Search

Despite the increasing abundance of whole transcriptome data, few methods are available to analyze global gene expression across phylogenies. Here, we present a new software package (Computational Analysis of Gene Expression Evolution [CAGEE]) for inferring patterns of increases and decreases in gene expression across a phylogenetic tree, as well as the rate at which these changes occur. In contrast to previous methods that treat each gene independently, CAGEE can calculate genome-wide rates of gene expression, along with ancestral states for each gene. The statistical approach developed here makes it possible to infer lineage-specific shifts in rates of evolution across the genome, in addition to possible differences in rates among multiple tissues sampled from the same species. We demonstrate the accuracy and robustness of our method on simulated data and apply it to a data set of ovule gene expression collected from multiple self-compatible and self-incompatible species in the genus Solanum to test hypotheses about the evolutionary forces acting during mating system shifts. These comparisons allow us to highlight the power of CAGEE, demonstrating its utility for use in any empirical system and for the analysis of most morphological traits. Our software is available at https://github.com/hahnlab/CAGEE/. [ABSTRACT FROM AUTHOR]

Mismatches between parental genomes in selfish elements are frequently hypothesized to underlie hybrid dysfunction and drive speciation. However, because the genetic basis of most hybrid incompatibilities is unknown, testing the contribution of selfish elements to reproductive isolation is difficult. Here, we evaluated the role of transposable elements (TEs) in hybrid incompatibilities between Drosophila virilis and D. lummei by experimentally comparing hybrid incompatibility in a cross where active TEs are present in D. virilis (TE+) and absent in D. lummei, to a cross where these TEs are absent from both D. virilis (TE−) and D. lummei genotypes. Using genomic data, we confirmed copy number differences in TEs between the D. virilis (TE+) strain and both the D. virilis (TE−) strain and D. lummei. We observed F1 postzygotic reproductive isolation exclusively in the interspecific cross involving TE+ D. virilis but not in crosses involving TE− D. virilis. This mirrors intraspecies dysgenesis where atrophied testes only occur when TE+ D. virilis is the paternal parent. A series of backcross experiments, that accounted for alternative models of hybrid incompatibility, showed that both F1 hybrid incompatibility and intrastrain dysgenesis are consistent with the action of TEs rather than genic interactions. Thus, our data suggest that this TE mechanism manifests as two different incompatibility phenotypes. A further Y‐autosome interaction contributes to additional, sex‐specific, inviability in one direction of this cross‐combination. These experiments demonstrate that TEs that cause intraspecies dysgenesis can increase reproductive isolation between closely related lineages, thereby adding to the processes that consolidate speciation. [ABSTRACT FROM AUTHOR]

Drosophila pseudoobscura females that co‐occur with sister species D. persimilis show elevated fertilization by conspecific sperm when they mate with both a heterospecific and a conspecific male. This phenomenon, known as conspecific sperm precedence (CSP), has evolved as a mechanism to avoid maladaptive hybridization with D. persimilis. In this study, we assessed pericopulatory (during mating) and postcopulatory (after mating) traits in crosses with sympatric or allopatric D. pseudoobscura females and conspecific or heterospecific males to evaluate potential mechanisms of CSP in this system. We observed shorter copulation duration in crosses with sympatric females, but found no difference in quantity of sperm transferred or female reproductive tract toxicity between sympatry and allopatry. Our data show some support for the hypothesis that parasperm, a short, sterile sperm morph, can protect fertile eusperm from the D. pseudoobscura female reproductive tract, though it is unclear how this might affect patterns of sperm use in sympatry vs. allopatry. Overall, these results suggest that copulation duration could potentially contribute to the elevated CSP observed in sympatry. [ABSTRACT FROM AUTHOR]

Because sensory signals often evolve rapidly, they could be instrumental in the emergence of reproductive isolation between species. However, pinpointing their specific contribution to isolating barriers, and the mechanisms underlying their divergence, remains challenging. Here, we demonstrate sexual isolation due to divergence in chemical signals between two populations of Drosophila americana (SC and NE) and one population of D. novamexicana, and dissect its underlying phenotypic and genetic mechanisms. Mating trials revealed strong sexual isolation between Drosophila novamexicana males and SC Drosophila americana females, as well as more moderate bi‐directional isolation between D. americana populations. Mating behavior data indicate SC D. americana males have the highest courtship efficiency and, unlike males of the other populations, are accepted by females of all species. Quantification of cuticular hydrocarbon (CHC) profiles—chemosensory signals that are used for species recognition and mate finding in Drosophila—shows that the SC D. americana population differs from the other populations primarily on the basis of compound carbon chain‐length. Moreover, manipulation of male CHC composition via heterospecific perfuming—specifically perfuming D. novamexicana males with SC D. americana males—abolishes their sexual isolation from these D. americana females. Of a set of candidates, a single gene—elongase CG17821—had patterns of gene expression consistent with a role in CHC differences between species. Sequence comparisons indicate D. novamexicana and our Nebraska (NE) D. americana population share a derived CG17821 truncation mutation that could also contribute to their shared "short" CHC phenotype. Together, these data suggest an evolutionary model for the origin and spread of this allele and its consequences for CHC divergence and sexual isolation in this group. [ABSTRACT FROM AUTHOR]

Dissecting the genetic mechanisms underlying dioecy (i.e. separate female and male individuals) is critical for understanding the evolution of this pervasive reproductive strategy. Nonetheless, the genetic basis of sex determination remains unclear in many cases, especially in systems where dioecy has arisen recently. Within the economically important plant genus Solanum (∼2,000 species), dioecy is thought to have evolved independently at least 4 times across roughly 20 species. Here, we generate the first genome sequence of a dioecious Solanum and use it to ascertain the genetic basis of sex determination in this species. We de novo assembled and annotated the genome of Solanum appendiculatum (assembly size: ∼750 Mb scaffold N50: 0.92 Mb; ∼35,000 genes), identified sex-specific sequences and their locations in the genome, and inferred that males in this species are the heterogametic sex. We also analyzed gene expression patterns in floral tissues of males and females, finding approximately 100 genes that are differentially expressed between the sexes. These analyses, together with observed patterns of gene-family evolution specific to S. appendiculatum , consistently implicate a suite of genes from the regulatory network controlling pectin degradation and modification in the expression of sex. Furthermore, the genome of a species with a relatively young sex-determination system provides the foundational resources for future studies on the independent evolution of dioecy in this clade. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

An increasing number of phylogenomic studies have documented a clear "footprint" of postspeciation introgression among closely related species. Nonetheless, systematic genome‐wide studies of factors that determine the likelihood of introgression remain rare. Here, we propose an a priori hypothesis‐testing framework that uses introgression statistics—including a new metric of estimated introgression, Dp—to evaluate general patterns of introgression prevalence and direction across multiple closely related species. We demonstrate this approach using whole genome sequences from 32 lineages in 11 wild tomato species to assess the effect of three factors on introgression—genetic relatedness, geographical proximity, and mating system differences—based on multiple trios within the "ABBA–BABA" test. Our analyses suggest each factor affects the prevalence of introgression, although our power to detect these is limited by the number of comparisons currently available. We find that of 14 species pairs with geographically "proximate" versus "distant" population comparisons, 13 showed evidence of introgression; in 10 of these cases, this was more prevalent between geographically closer populations. We also find modest evidence that introgression declines with increasing genetic divergence between lineages, is more prevalent between lineages that share the same mating system, and—when it does occur between mating systems—tends to involve gene flow from more inbreeding to more outbreeding lineages. Although our analysis indicates that recent postspeciation introgression is frequent in this group—detected in 15 of 17 tested trios—estimated levels of genetic exchange are modest (0.2–2.5% of the genome), so the relative importance of hybridization in shaping the evolutionary trajectories of these species could be limited. Regardless, similar clade‐wide analyses of genomic introgression would be valuable for disentangling the major ecological, reproductive, and historical determinants of postspeciation gene flow, and for assessing the relative contribution of introgression as a source of genetic variation. [ABSTRACT FROM AUTHOR]

The Galápagos Islands are home to incredible endemic biodiversity that is of high conservation interest. Two such endemic species are the Galápagos tomatoes: Solanum cheesmaniae and Solanum galapagense. Both are known from historical location records, but like many endemic plant species on the Galápagos, their current conservation status is unclear. We revisited previously documented sites of endemic species on San Cristóbal, Santa Cruz, and Isabela, and document the disappearance of > 80% of these populations. In contrast, we find that two invasive relatives (Solanum pimpinellifolium and Solanum lycopersicum) are now highly abundant, and in some cases—based on morphological observations—might be hybridizing with endemics. Our findings suggest that expanding human developments and putative interspecific hybridization are among the major factors affecting the prevalence of invasives and the threatened persistence of the endemic populations. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

Summary: 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. [ABSTRACT FROM AUTHOR]

Within the economically important plant family Solanaceae, Jaltomata is a rapidly evolving genus that has extensive diversity in flower size and shape, as well as fruit and nectar color, among its ∼80 species. Here, we report the whole-genome sequencing, assembly, and annotation, of one representative species (Jaltomata sinuosa) from this genus. Combining PacBio long reads (25×) and Illumina short reads (148×) achieved an assembly of ∼1.45 Gb, spanning ∼96% of the estimated genome. Ninety-six percent of curated single-copy orthologs in plants were detected in the assembly, supporting a high level of completeness of the genome. Similar to other Solanaceous species, repetitive elements made up a large fraction (∼80%) of the genome, with the most recently active element, Gypsy, expanding across the genome in the last 1–2 Myr. Computational gene prediction, in conjunction with a merged transcriptome data set from 11 tissues, identified 34,725 protein-coding genes. Comparative phylogenetic analyses with six other sequenced Solanaceae species determined that Jaltomata is most likely sister to Solanum, although a large fraction of gene trees supported a conflicting bipartition consistent with substantial introgression between Jaltomata and Capsicum after these species split. We also identified gene family dynamics specific to Jaltomata, including expansion of gene families potentially involved in novel reproductive trait development, and loss of gene families that accompanied the loss of self-incompatibility. This high-quality genome will facilitate studies of phenotypic diversification in this rapidly radiating group and provide a new point of comparison for broader analyses of genomic evolution across the Solanaceae. [ABSTRACT FROM AUTHOR]

Abstract: Phylogenetic analyses of trait evolution can provide insight into the evolutionary processes that initiate and drive phenotypic diversification. However, recent phylogenomic studies have revealed extensive gene tree–species tree discordance, which can lead to incorrect inferences of trait evolution if only a single species tree is used for analysis. This phenomenon—dubbed “hemiplasy”—is particularly important to consider during analyses of character evolution in rapidly radiating groups, where discordance is widespread. Here, we generate whole‐transcriptome data for a phylogenetic analysis of 14 species in the plant genus Jaltomata (the sister clade to Solanum), which has experienced rapid, recent trait evolution, including in fruit and nectar colour, and flower size and shape. Consistent with other radiations, we find evidence for rampant gene tree discordance due to incomplete lineage sorting (ILS) and to introgression events among the well‐supported subclades. As both ILS and introgression increase the probability of hemiplasy, we perform several analyses that take discordance into account while identifying genes that might contribute to phenotypic evolution. Despite discordance, the history of fruit colour evolution in Jaltomata can be inferred with high confidence, and we find evidence of de novo adaptive evolution at individual genes associated with fruit colour variation. In contrast, hemiplasy appears to strongly affect inferences about floral character transitions in Jaltomata, and we identify candidate loci that could arise either from multiple lineage‐specific substitutions or standing ancestral polymorphisms. Our analysis provides a generalizable example of how to manage discordance when identifying loci associated with trait evolution in a radiating lineage. [ABSTRACT FROM AUTHOR]

Background: Heterochronic shifts during mid- to late stages of organismal development have been proposed as key mechanisms generating phenotypic diversity. To determine whether late heterochronic shifts underlie derived floral morphologies within Jaltomata (Solanaceae)--a genus whose species have extensive and recently evolved floral diversity--we compared floral development of four diverse species (including an ambiguously ancestral or secondarily derived rotate, two putatively independently evolved campanulate, and a tubular morph) to the ancestral rotate floral form, as well as to an outgroup that shares this ancestral floral morphology. Results: We determined that early floral development (< 1 mm bud diameter, corresponding to completion of organ whorl initiation) is very similar among all species, but that different mature floral forms are distinguishable by mid-development (> 1 mm diameter) due to differential growth acceleration of corolla traits. Floral ontogeny among similar mature rotate forms remains comparable until late stages, while somewhat different patterns of organ growth are found between species with similar campanulate forms. Conclusions: Our data suggest shared floral patterning during early-stage development, but that different heterochronic shifts during mid- and late-stage development contribute to divergent floral traits. Heterochrony thus appears to have been important in the rapid and repeated diversification of Jaltomata flowers. [ABSTRACT FROM AUTHOR]

Species barriers, expressed as hybrid inviability and sterility, are often due to epistatic interactions between divergent loci from two lineages. Theoretical models indicate that the strength, direction, and complexity of these genetic interactions can strongly affect the expression of interspecific reproductive isolation and the rates at which new species evolve. Nonetheless, empirical analyses have not quantified the frequency with which loci are involved in interactions affecting hybrid fitness, and whether these loci predominantly interact synergistically or antagonistically, or preferentially involve loci that have strong individual effects on hybrid fitness. We systematically 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), using lines containing pairwise combinations of 15 chromosomal segments from S. habrochaites in the background of S. lycopersicum (i.e., 95 double introgression lines). We compared the strength of hybrid incompatibility (either pollen sterility or seed sterility) expressed in each double introgression line to the expected additive effect of its two component single introgressions. We found that epistasis was common among co-introgressed regions. Interactions for hybrid dysfunction were substantially more prevalent in pollen fertility compared to seed fertility phenotypes, and were overwhelmingly antagonistic (i.e., double hybrids were less unfit than expected from additive single introgression effects). This pervasive antagonism is expected to attenuate the rate at which hybrid infertility accumulates among lineages over time (i.e., giving diminishing returns as more reproductive isolation loci accumulate), as well as decouple of patterns of accumulation of sterility loci and hybrid incompatibility phenotypes. This decoupling effect might explain observed differences between pollen and seed fertility in their fit to theoretical predictions of the accumulation of isolation loci, including the ‘snowball’ effect. [ABSTRACT FROM AUTHOR]

Divergence in phenotypic traits often contributes to premating isolation between lineages, but could also promote isolation at postmating stages. Phenotypic differences could directly result in mechanical isolation or hybrids with maladapted traits; alternatively, when alleles controlling these trait differences pleiotropically affect other components of development, differentiation could indirectly produce genetic incompatibilities in hybrids. Here, we determined the strength of nine postmating and intrinsic postzygotic reproductive barriers among 10 species of Jaltomata (Solanaceae), including species with highly divergent floral traits. To evaluate the relative importance of floral trait diversification for the strength of these postmating barriers, we assessed their relationship to floral divergence, genetic distance, geographical context, and ecological differences, using conventional tests and a new linear-mixed modeling approach. Despite close evolutionary relationships, all species pairs showed moderate to strong isolation. Nonetheless, floral trait divergence was not a consistent predictor of the strength of isolation; instead this was best explained by genetic distance, although we found evidence for mechanical isolation in one species, and a positive relationship between floral trait divergence and fruit set isolation across species pairs. Overall, our data indicate that intrinsic postzygotic isolation is more strongly associated with genome-wide genetic differentiation, rather than floral divergence. [ABSTRACT FROM AUTHOR]

Reinforcement occurs when hybridization between closely related lineages produces low-fitness offspring, prompting selection for elevated reproductive isolation specifically in areas of sympatry. Both premating and postmating prezygotic behaviors have been shown to be the target of reinforcing selection, but it remains unclear whether remating behaviors experience reinforcement, although they can also influence offspring identity and limit formation of hybrids. Here, we evaluated evidence for reinforcing selection on remating behaviors in Drosophila pseudoobscura, by comparing remating traits in females from populations historically allopatric and sympatric with Drosophila persimilis. We found that the propensity to remate was not higher in sympatric females, compared to allopatric females, regardless of whether the first mated male was heterospecific or conspecific. Moreover, remating behavior did not contribute to interspecific reproductive isolation among any population; that is, females showed no higher propensity to remate following a heterospecific first mating than following a conspecific first mating. Instead, we found that females are less likely to remate after initial matings with unfamiliar males, regardless of species identity. This is consistent with one scenario of postmating sexual conflict in which females are poorly defended against postcopulatory manipulation by males with whom they have not coevolved. Our results are generally inconsistent with reinforcement on remating traits and suggest that this behavior might be more strongly shaped by the consequences of local antagonistic male-female interactions than interactions with heterospecifics. [ABSTRACT FROM AUTHOR]

Little is known about the physiological responses and genetic mutations associated with reproductive isolation between species, especially for postmating prezygotic isolating barriers. Here, we examine changes in gene expression that accompany the expression of 'unilateral incompatibility' ( UI)-a postmating prezygotic barrier in which fertilization is prevented by gamete rejection in the reproductive tract [in this case of pollen tubes (male gametophytes)] in one direction of a species cross, but is successful in the reciprocal crossing direction. We use whole-transcriptome sequencing of multiple developmental stages of male and female tissues in two Solanum species that exhibit UI to: (i) identify transcript differences between UI-competent and UI noncompetent tissues; (ii) characterize transcriptional changes specifically associated with the phenotypic expression of UI; and (iii) using these comparisons, evaluate the behaviour of a priori candidate loci for UI and identify new candidates for future manipulative work. In addition to describing transcriptome-wide changes in gene expression that accompany this isolating barrier, we identify at least five strong candidates for involvement in postmating prezygotic incompatibility between species. These include three novel candidates and two candidates that are strongly supported by prior developmental, functional, and quantitative trait locus mapping studies. These latter genes are known molecular players in the intraspecific expression of mate choice via genetic self-incompatibility, and our study supports prior evidence that these inter- and intraspecific postmating prezygotic reproductive behaviours share specific genetic and molecular mechanisms. [ABSTRACT FROM AUTHOR]

Cascade speciation and reinforcement can evolve rapidly when traits are pleiotropic and act as both signal/cue in nonrandommating. Here, we examine the contribution of two key traits--assortative mating and self-fertilization--to reinforcement and (by extension) cascade speciation. First, using a population genetic model of reinforcement we find that both assortative mating and self-fertilization can make independent contributions to increased reproductive isolation, consistent with reinforcement. Self-fertilization primarily evolves due to its 2-fold transmission advantage when inbreeding depression (d) is lower (d<0.45) but evolves as a function of the cost of hybridization under higher inbreeding depression (0.45

Understanding the genetic basis for changes in transcriptional regulation is an important aspect of understanding phenotypic evolution. Using interspecific introgression lines, we infer the mechanisms of divergence in genome-wide patterns of gene expression between the nightshades Solanum pennellii and S. lycopersicum (domesticated tomato). We find that cis- and trans-regulatory changes have had qualitatively similar contributions to divergence in this clade, unlike results from other systems. Additionally, expression data from four tissues (shoot apex, ripe fruit, pollen, and seed) suggest that introgressed regions in these hybrid lines tend to be downregulated, while background (nonintrogressed) genes tend to be upregulated. Finally, we find no evidence for an association between the magnitude of differential expression in NILs and previously determined sterility phenotypes. Our results contradict previous predictions of the predominant role of cis- over trans-regulatory divergence between species, and do not support a major role for gross genome-wide misregulation in reproductive isolation between these species. [ABSTRACT FROM AUTHOR]

Speciation events often occur in rapid bursts of diversification, but the ecological and genetic factors that promote these radiations are still much debated. Using whole transcriptomes from all 13 species in the ecologically and reproductively diverse wild tomato clade (Solanum sect. Lycopersicon), we infer the species phylogeny and patterns of genetic diversity in this group. Despite widespread phylogenetic discordance due to the sorting of ancestral variation, we date the origin of this radiation to approximately 2.5 million years ago and find evidence for at least three sources of adaptive genetic variation that fuel diversification. First, we detect introgression both historically between early-branching lineages and recently between individual populations, at specific loci whose functions indicate likely adaptive benefits. Second, we find evidence of lineage-specific de novo evolution for many genes, including loci involved in the production of red fruit color. Finally, using a “PhyloGWAS” approach, we detect environment-specific sorting of ancestral variation among populations that come from different species but share common environmental conditions. Estimated across the whole clade, small but substantial and approximately equal fractions of the euchromatic portion of the genome are inferred to contribute to each of these three sources of adaptive genetic variation. These results indicate that multiple genetic sources can promote rapid diversification and speciation in response to new ecological opportunity, in agreement with our emerging phylogenomic understanding of the complexity of both ancient and recent species radiations. [ABSTRACT FROM AUTHOR]

Despite extensive theory, little is known about the empirical accumulation and evolutionary timing of mutations that contribute to speciation. Here we combined QTL (Quantitative Trait Loci) analyses of reproductive isolation, with information on species evolutionary relationships, to reconstruct the order and timing of mutations contributing to reproductive isolation between three plant (Solanum) species. To evaluate whether reproductive isolation QTL that appear to coincide in more than one species pair are homologous, we used cross-specific tests of allelism and found evidence for both homologous and lineage-specific (non-homologous) alleles at these co-localized loci. These data, along with isolation QTL unique to single species pairs, indicate that >85% of isolation-causing mutations arose later in the history of divergence between species. Phylogenetically explicit analyses of these data support non-linear models of accumulation of hybrid incompatibility, although the specific best-fit model differs between seed (pairwise interactions) and pollen (multi-locus interactions) sterility traits. Our findings corroborate theory that predicts an acceleration (‘snowballing’) in the accumulation of isolation loci as lineages progressively diverge, and suggest different underlying genetic bases for pollen versus seed sterility. Pollen sterility in particular appears to be due to complex genetic interactions, and we show this is consistent with a snowball model where later arising mutations are more likely to be involved in pairwise or multi-locus interactions that specifically involve ancestral alleles, compared to earlier arising mutations. [ABSTRACT FROM AUTHOR]

Plant defense traits can be shaped by evolutionary and physiological constraints, as well as local ecological selection. We assessed the relative importance of these factors in shaping defense trait variation across the wild tomato clade (a group of 13 closely related species) using an herbivore bioassay (Manduca sexta). With phylogenetic comparative methods, we evaluated patterns of constitutive and induced defense variation, and the extent of coupling between alternative defense strategies. We detected substantial variation among species and found no evidence for phylogenetic conservatism among defensive traits, unlike for two other ecologically relevant (reproductive) traits. In addition, constitutive and induced defense syndromes were unassociated. These data indicate that, in this group, there is no evidence for either phylogenetic conservatism of shared consumer guilds that shape defense traits, or for constraints on defense trait evolution, including mechanistic trade-offs between defense strategies. Our data suggest that defense trait variation in this clade instead results from rapid responses to local ecological conditions. [ABSTRACT FROM AUTHOR]

Natural selection on photosynthetic performance is a primary factor determining leaf phenotypes. The complex CO2 diffusion path from substomatal cavities to the chloroplasts - the mesophyll conductance ( gm) - limits photosynthetic rate in many species and hence shapes variation in leaf morphology and anatomy. Among sclerophyllous and succulent taxa, structural investment in leaves, measured as the leaf dry mass per area ( LMA), has been implicated in decreased gm. However, in herbaceous taxa with high gm, it is less certain how LMA impacts CO2 diffusion and whether it significantly affects photosynthetic performance. We addressed these questions in the context of understanding the ecophysiological significance of leaf trait variation in wild tomatoes, a closely related group of herbaceous perennials. Although gm was high in wild tomatoes, variation in gm significantly affected photosynthesis. Even in these tender-leaved herbaceous species, greater LMA led to reduced gm. This relationship between gm and LMA is partially mediated by cell packing and leaf thickness, although amphistomy (equal distribution of stomata on both sides of the leaf) mitigates the effect of leaf thickness. Understanding the costs of increased LMA will inform future work on the adaptive significance of leaf trait variation across ecological gradients in wild tomatoes and other systems. [ABSTRACT FROM AUTHOR]

We examined reproductive isolating barriers at four postmating stages among 11 species from the morphologically diverse genus Nolana (Solanaceae). At least one stage was positively correlated with both genetic and geographic distance between species. Postzygotic isolation was generally stronger and faster evolving than postmating prezygotic isolation. In addition, there was no evidence for mechanical isolation, or for reproductive character displacement in floral traits that can influence pollinator isolation. In general, among the potential isolating stages examined here, postzygotic barriers appear to be more effective contributors to reducing gene flow, including between sympatric species. [ABSTRACT FROM AUTHOR]

Summary The cuticle covers the aerial epidermis of land plants and plays a primary role in water regulation and protection from external stresses. Remarkable species diversity in the structure and composition of its components, cutin and wax, have been catalogued, but few functional or genetic correlations have emerged. Tomato ( Solanum lycopersicum) is part of a complex of closely related wild species endemic to the northern Andes and the Galapagos Islands ( Solanum Sect. Lycopersicon). Although sharing an ancestor <7 million years ago, these species are found in diverse environments and are subject to unique selective pressures. Furthermore, they are genetically tractable, since they can be crossed with S. lycopersicum, which has a sequenced genome. With the aim of evaluating the relationships between evolution, structure and function of the cuticle, we characterized the morphological and chemical diversity of fruit cuticles of seven species from Solanum Sect. Lycopersicon. Striking differences in cuticular architecture and quantities of cutin and waxes were observed, with the wax coverage of wild species exceeding that of S. lycopersicum by up to seven fold. Wax composition varied in the occurrence of wax esters and triterpenoid isomers. Using a Solanum habrochaites introgression line population, we mapped triterpenoid differences to a genomic region that includes two S. lycopersicum triterpene synthases. Based on known metabolic pathways for acyl wax compounds, hypotheses are discussed to explain the appearance of wax esters with atypical chain lengths. These results establish a model system for understanding the ecological and evolutionary functional genomics of plant cuticles. [ABSTRACT FROM AUTHOR]

Genome scans have become a common approach to identify genomic signatures of natural selection and reproductive isolation, as well as the genomic bases of ecologically relevant phenotypes, based on patterns of polymorphism and differentiation among populations or species. Here, we review the results of studies taking genome scan approaches in plants, consider the patterns of genomic differentiation documented and their possible causes, discuss the results in light of recent models of genomic differentiation during divergent adaptation and speciation, and consider assumptions and caveats in their interpretation. We find that genomic regions of high divergence generally appear quite small in comparisons of both closely and more distantly related populations, and for the most part, these differentiated regions are spread throughout the genome rather than strongly clustered. Thus, the genome scan approach appears well-suited for identifying genomic regions or even candidate genes that underlie adaptive divergence and/or reproductive barriers. We consider other methodologies that may be used in conjunction with genome scan approaches, and suggest further developments that would be valuable. These include broader use of sequence-based markers of known genomic location, greater attention to sampling strategies to make use of parallel environmental or phenotypic transitions, more integration with approaches such as quantitative trait loci mapping and measures of gene flow across the genome, and additional theoretical and simulation work on processes related to divergent adaptation and speciation. [ABSTRACT FROM AUTHOR]

New models of TE repression in plants (specifically Arabidopsis) have suggested specific mechanisms by which TE misregulation in hybrids might result in the expression of hybrid inviability. If true, these models suggest as yet undescribed consequences for (1) mechanistic connections between hybrid problems expressed at different postzygotic stages (e.g., inviability versus sterility), (2) the predicted strength, stage, and direction of isolation between diverging lineages that differ in TE activity, and (3) the association between species attributes that influence TE dynamics (e.g., mode of reproduction, geographical structure) and the rate at which they could accumulate incompatibilities. In this paper, we explore these implications and outline future empirical directions for generating data necessary to evaluate them. [ABSTRACT FROM AUTHOR]

Although traditionally separated by different aims and methodologies, research on agricultural and evolutionary problems shares a common goal of understanding the mechanisms underlying functionally important traits. As such, research in both fields offers potential complementary and reciprocal insights. Here, we discuss adaptive stress responses (specifically to water stress) as an example of potentially fruitful research reciprocity, where agricultural research has clearly produced advances that could benefit evolutionary studies, while evolutionary studies offer approaches and insights underexplored in crop studies. We focus on research on Solanum species that include the domesticated tomato and its wild relatives. Integrated approaches to understanding ecological adaptation are particularly attractive in tomato and its wild relatives: many presumptively adaptive phenotypic differences characterize wild species, and the physiological and mechanistic basis of many relevant traits and environmental responses has already been examined in the context of cultivated tomato and some wild species. We highlight four specific instances where these reciprocal insights can be combined to better address questions that are fundamental both to agriculture and evolution. [ABSTRACT FROM AUTHOR]

The two “rules of speciation”—the Large X-effect and Haldane's rule—hold throughout the animal kingdom, but the underlying genetic mechanisms that cause them are still unclear. Two predominant explanations—the “dominance theory” and faster male evolution—both have some empirical support, suggesting that the genetic basis of these rules is likely multifarious. We revisit one historical explanation for these rules, based on dysfunctional genetic interactions involving genes recently moved between chromosomes. We suggest that gene movement specifically off or onto the X chromosome is another mechanism that could contribute to the two rules, especially as X chromosome movements can be subject to unique sex-specific and sex chromosome specific consequences in hybrids. Our hypothesis is supported by patterns emerging from comparative genomic data, including a strong bias in interchromosomal gene movements involving the X and an overrepresentation of male reproductive functions among chromosomally relocated genes. In addition, our model indicates that the contribution of gene movement to the two rules in any specific group will depend upon key developmental and reproductive parameters that are taxon specific. We provide several testable predictions that can be used to assess the importance of gene movement as a contributor to these rules in the future. [ABSTRACT FROM AUTHOR]

Understanding the role of geography and ecology in species divergence is central to the study of evolutionary diversification. We used climatic, geographic, and biological data from nine wild Andean tomato species to describe each species' ecological niche and to evaluate the likely ecological and geographical modes of speciation in this clade. Using data from >1000 wild accessions and publicly available data derived from geographic information systems for various environmental variables, we found most species pairs were significantly differentiated for one or more environmental variables. By comparing species' predicted niches generated by species distribution modeling (SDM), we found significant niche differentiation among three of four sister-species pairs, suggesting ecological divergence is consistently associated with recent divergence. In comparison, based on age-range correlation (ARC) analysis, there was no evidence for a predominant geographical (allopatric vs. sympatric) context for speciation in this group. Overall, our results suggest an important role for environmentally mediated differentiation, rather than simply geographical isolation, in species divergence. [ABSTRACT FROM AUTHOR]

• Epistasis, the nonadditive interaction between loci, is thought to play a role in many fundamental evolutionary processes, including adaptive differentiation and speciation. Focusing on species differences in ecophysiological traits, we examined the strength and direction of pairwise epistatic interactions between target chromosomal regions from one species, when co-introgressed into the genetic background of a foreign species. • A full diallel cross was performed using 15 near-isogenic lines (NILs) constructed between two tomato species ( Solanum habrochaites and Solanum lycopersicum) to compare the phenotypic effects of each chromosomal region singly and in combination with each other region. • We detected main effect quantitative trait loci (QTLs) for two of our three focal traits. Epistatic effects accounted for c. 25% of detected effects on trait means, depending on the trait. Strikingly, all but two interactions were antagonistic, with the combined effect of chromosomal regions acting in the opposite direction from that of one or both individual chromosomal regions. • Our study is one of the few to systematically examine pairwise epistatic effects in a nonmicrobial system. Our results suggest that epistatic interactions can contribute substantially to the genetic basis of traits involved in adaptive species differentiation, especially highly complex, multivariate traits. [ABSTRACT FROM AUTHOR]

The plant group Solanum section Lycopersicon (the clade containing the domesticated tomato and its wild relatives) is ideal for integrating genomic tools and approaches into ecological and evolutionary research. Wild species within Lycopersicon span broad morphological, physiological, life history, mating system, and biochemical variation, and are separated by substantial, but incomplete postmating reproductive barriers, making this an ideal system for genetic analyses of these traits. This ecological and evolutionary diversity is matched by many logistical advantages, including extensive historical occurrence records for all species in the group, publicly available germplasm for hundreds of known wild accessions, demonstrated experimental tractability, and extensive genetic, genomic, and functional tools and information from the tomato research community. Here I introduce the numerous advantages of this system for Ecological and Evolutionary Functional Genomics (EEFG), and outline several ecological and evolutionary phenotypes and questions that can be fruitfully tackled in this system. These include biotic and abiotic adaptation, reproductive trait evolution, and the genetic basis of speciation. With the modest enhancement of some research strengths, this system is poised to join the best of our currently available model EEFG systems. [ABSTRACT FROM AUTHOR]

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. [ABSTRACT FROM AUTHOR]

I compare the genetic basis of quantitative traits that potentially contribute to pre- and postzygotic isolation between the plant species Solanum lycopersicum (formerly Lycopersicon esculentum) and Solanum habrochaites (formerly Lycopersicon hirsutum), using quantitative trait loci (QTL) mapping in a set of near-isogenic lines. Putative prezygotic isolating traits include flower size, flower shape, stigma exsertion, and inflorescence length, that can influence pollinator preferences and/or selfing rates, and therefore gene flow between divergent types. Postzygotic isolating traits are hybrid pollen and seed sterility. Three substantive results emerge from these analyses. First, the genetic basis of floral differentiation appears to be somewhat less complex than the genetic basis of postzygotic hybrid sterility, although these differences are very modest. Second, there is little evidence that traits for floral differentiation are causally or mechanistically associated with hybrid sterility traits in this species cross. Third, there is little evidence that hybrid sterility QTL are more frequently associated with chromosomal centromeric regions, in comparison to floral trait QTL, a prediction of centromeric drive models of hybrid sterility. Although genome-wide associations are not evident in this analysis, several individual chromosomal regions that contain clusters of QTL for both floral and sterility traits, or that indicate hybrid sterility effects at centromere locations, warrant further fine-scale investigation. [ABSTRACT FROM AUTHOR]

The contemporary pattern of intraspecific genetic variation can indicate the relative role of gene flow and local differentiation in shaping the evolutionary history and future trajectory of a species. To assess the recent influence of contrasting life history and demographic characteristics on genetic structure within a group of closely related species, patterns of genetic differentiation ( FST and related statistics) and isolation by distance (IBD) were compared among 17 congeneric herbaceous plant species. Data came from 35 published studies of 16 species, and a previously unpublished analysis of chloroplast genetic variation in the rare endemic Silene rotundifolia. Among-population genetic variance was most strongly influenced by the type of genetic marker used; cytoplasmic markers showed larger values than allozyme and anonymous nuclear markers. Other independently significant factors were geographical range size and, for allozyme studies, reproductive system; in particular, endemism and hermaphroditism were associated with higher among-population genetic variance, whereas large native geographical range and dioecy were associated with lower among-population variance. Over equivalent spatial scales, dioecious populations also showed weaker IBD than hermaphrodites, perhaps because increased population transience and/or variance in the spatial pattern of gene flow are more closely associated with dioecy in this genus. Invasive populations had both highly variable among-population genetic variance, and no evidence for IBD, consistent with nonequilibrium conditions. Other analysed factors including predominant pollinator had no discernable influence on genetic structure or patterns of IBD. In general, this comparative approach appears to be valuable for synthesizing the complementary information provided by F-statistics and IBD, and for indicating the relative importance of particular biological factors in shaping genetic variation within different species of a closely related plant group. [ABSTRACT FROM AUTHOR]

Analyses among animal species have found that reproductive isolation increases monotonically with genetic distance, evolves more quickly for prezygotic than postzygotic traits, and is stronger among sympatric than allopatric species pairs. The latter pattern is consistent with expectations under the reinforcement hypothesis. To determine whether similar trends are found among plant species, patterns of reproductive isolation (postpollination prezygotic, postzygotic, and "total" isolation) in three plant genera (Glycine, Silene, Streptanthus) were examined using data from previously published artificial hybridization experiments. In Silene, all measures of reproductive isolation were positively correlated with genetic distance. In contrast, in Glycine and Streptanthus, correlations between reproductive isolation and genetic distance were weak or nonsignificant, possibly due to the influence of biologically unusual taxa, variable evolutionary forces acting in different lineages, or insufficient time to accumulate reproductive isolation. There was no evidence that postpollination prezygotic reproductive isolation evolved faster than postzygotic isolation in Glycine or Silene. We also detected no evidence for faster accumulation of postmating prezygotic isolation between sympatric than allopatric species pairs; thus we found no evidence for the operation of speciation via reinforcement. In Silene, which included six polyploid species, results suggest that changes in ploidy disrupt a simple monotonic relationship between isolation and genetic distance. [ABSTRACT FROM AUTHOR]

The article focuses on the Population Viability Analysis (PVA) in endangered species recovery plans in the U.S. It examines the role that PVA has played in recovery planning and management of rare species. The study suggests how the use of PVA in endangered species recovery planning might be improved in the future.

This article discusses research, presented elsewhere in this issue, focusing on the causes of species differentiation, or speciation. This research approaches the question of speciation in plants from the perspective of evolutionary biology by studying the causes of pollen and ovule sterility between closely related species. The causes of hybrid inviability and sterility in the relationship between Asian and African rice species are described. The implications of this research for the understanding of the role of selfish genes and postzygotic reproductive isolation in speciation.

The affiliation of the second author was incorrectly published in the original article. [ABSTRACT FROM AUTHOR]

Stress response mechanisms are ubiquitous and important for adaptation to heterogenous environments and could be based on constitutive or plastic responses to environmental stressors. Here we quantify constitutive and plastic gene expression differences under ambient and desiccation stress treatments, in males and females of three species of Drosophila known to differ in desiccation resistance. Drosophila novamexicana survives desiccation trials significantly longer than the two subspecies of Drosophila americana, consistent with its natural species range in the desert southwest USA. We found that desiccation stress reduces global expression differences between species—likely because many general stress response mechanisms are shared among species—but that all species showed plastic expression changes at hundreds of loci during desiccation. Nonetheless, D. novamexicana had the fewest genes with significant plastic expression changes, despite having the highest desiccation resistance. Of the genes that were significantly differentially expressed between species—either within each treatment (>200 loci), constitutively regardless of treatment (36 loci), or with different species-specific plasticity (26 loci)—GO analysis did not find significant enrichment of any major gene pathways or broader functions associated with desiccation stress. Taken together, these data indicate that if gene expression changes contribute to differential desiccation resistance between species, these differences are likely shaped by a relatively small set of influential genes rather than broad genome-wide differentiation in stress response mechanisms. Finally, among the set of genes with the greatest between-species plasticity, we identified an interesting set of immune-response genes with consistent but opposing reaction norms between sexes, whose potential functional role in sex-specific mechanisms of desiccation resistance remains to be determined. [ABSTRACT FROM AUTHOR]

Background: Disentangling the selective factors shaping adaptive trait variation is an important but challenging task. Many studies—especially in Drosophila—have documented trait variation along latitudinal or altitudinal clines, but frequently lack resolution about specific environmental gradients that could be causal selective agents, and often do not investigate covariation between traits simultaneously. Here we examined variation in multiple macroecological factors across geographic space and their associations with variation in three physiological traits (desiccation resistance, UV resistance, and pigmentation) at both population and species scales, to address the role of abiotic environment in shaping trait variation. Results: Using environmental data from collection locations of three North American Drosophila species—D. americana americana, D. americana texana and D. novamexicana—we identified two primary axes of macroecological variation; these differentiated species habitats and were strongly loaded for precipitation and moisture variables. In nine focal populations (three per species) assayed for each trait, we detected significant species-level variation for both desiccation resistance and pigmentation, but not for UV resistance. Species-level trait variation was consistent with differential natural selection imposed by variation in habitat water availability, although patterns of variation differed between desiccation resistance and pigmentation, and we found little evidence for pleiotropy between traits. Conclusions: Our multi-faceted approach enabled us to identify potential agents of natural selection and examine how they might influence the evolution of multiple traits at different evolutionary scales. Our findings highlight that environmental factors influence functional trait variation in ways that can be complex, and point to the importance of studies that examine these relationships at both population- and species-levels. [ABSTRACT FROM AUTHOR]

An introduction is presented in which the editor discusses various articles within the issue on topics including reproductive isolation in vertebrates, interspecific difference and heterospecific fertilization.

Arising from: J. B. Plotkin, J. Dushoff& H. B. Fraser 428, 942-945 (2004); see also communication from Nielsen et al.; Chen et al.; Plotkin et al. replyThe idea that natural selection on genes might be detected using only a single genome has been put forward by Plotkin and colleagues, who present a method that they claim can detect selection without the need for comparative data and which, if correct, would confer greater power of analysis with less information. Here we argue that their method depends on assumptions that confound their conclusions and that, even if these assumptions were valid, the authors' inferences about adaptive natural selection are unjustified. [ABSTRACT FROM AUTHOR]

Sexual selection and sexual conflict are considered important drivers of speciation, based on both theoretical models and empirical correlations between sexually selected traits and diversification. However, whether reproductive isolation between species evolves directly as a consequence of intrapopulation sexual dynamics remains empirically unresolved, in part because knowledge of the genetic mechanisms (if any) connecting these processes is limited. Here, we provide evidence of a direct mechanistic link between intraspecies sexual selection and reproductive isolation. We examined genes with known roles in intraspecific sperm competition (ISC) in D. melanogaster and assayed their impact on conspecific sperm precedence (CSP). We found that two such genes (Acp36DE and CG9997) contribute to both offensive sperm competition and CSP; null/knockdown lines both had lower competitive ability against D. melanogaster conspecifics and were no longer able to displace heterospecific D. simulans sperm in competitive matings. In comparison, Sex Peptide (Acp70A)—another locus essential for ISC—does not contribute to CSP. These data indicate that two loci important for sperm competitive interactions have an additional role in similar interactions that enforce post-mating reproductive isolation between species, and show that sexual selection and sexual isolation can act on the same molecular targets in a gene-specific manner. [ABSTRACT FROM AUTHOR]