The extent of introgression between incipient Clarkia species is determined by temporal environmental variation and mating system.

Introgression is pervasive across the tree of life but varies across taxa, geography, and genomic regions. However, the factors modulating this variation and how they may be affected by global change are not well understood. Here, we used 200 genomes and a 15-y site-specific environmental dataset to investigate the effects of environmental variation and mating system divergence on the magnitude of introgression between a recently diverged outcrosser-selfer pair of annual plants in the genus Clarkia. These sister taxa diverged very recently and subsequently came into secondary sympatry where they form replicated contact zones. Consistent with observations of other outcrosser-selfer pairs, we found that introgression was asymmetric between taxa, with substantially more introgression from the selfer to the outcrosser. This asymmetry was caused by a bias in the direction of initial F1 hybrid formation and subsequent backcrossing. We also found extensive variation in the outcrosser's admixture proportion among contact zones, which was predicted nearly entirely by interannual variance in spring precipitation. Greater fluctuations in spring precipitation resulted in higher admixture proportions, likely mediated by the effects of spring precipitation on the expression of traits that determine premating reproductive isolation. Climate-driven hybridization dynamics may be particularly affected by global change, potentially reshaping species boundaries and adaptation to novel environments.

A few genetic variants go a long way in differentiating Penstemon species.

The integrity of hybridizing species is usually maintained by genome-wide selection or by selection on a few genomic regions. A study published in PLOS Biology finds a different pattern-60 SNPs spread across the genome differentiate a Penstemon species pair.

Combined analysis of transposable elements and structural variation in maize genomes reveals genome contraction outpaces expansion.

Structural differences between genomes are a major source of genetic variation that contributes to phenotypic differences. Transposable elements, mobile genetic sequences capable of increasing their copy number and propagating themselves within genomes, can generate structural variation. However, their repetitive nature makes it difficult to characterize fine-scale differences in their presence at specific positions, limiting our understanding of their impact on genome variation. Domesticated maize is a particularly good system for exploring the impact of transposable element proliferation as over 70% of the genome is annotated as transposable elements. High-quality transposable element annotations were recently generated for de novo genome assemblies of 26 diverse inbred maize lines. We generated base-pair resolved pairwise alignments between the B73 maize reference genome and the remaining 25 inbred maize line assemblies. From this data, we classified transposable elements as either shared or polymorphic in a given pairwise comparison. Our analysis uncovered substantial structural variation between lines, representing both simple and complex connections between TEs and structural variants. Putative insertions in SNP depleted regions, which represent recently diverged identity by state blocks, suggest some TE families may still be active. However, our analysis reveals that within these recently diverged genomic regions, deletions of transposable elements likely account for more structural variation events and base pairs than insertions. These deletions are often large structural variants containing multiple transposable elements. Combined, our results highlight how transposable elements contribute to structural variation and demonstrate that deletion events are a major contributor to genomic differences.

Conflict over fertilization underlies the transient evolution of reinforcement.

When two species meet in secondary contact, the production of low fitness hybrids may be prevented by the adaptive evolution of increased prezygotic isolation, a process known as reinforcement. Theoretical challenges to the evolution of reinforcement are generally cast as a coordination problem, i.e., "how can statistical associations between traits and preferences be maintained in the face of recombination?" However, the evolution of reinforcement also poses a potential conflict between mates. For example, the opportunity costs to hybridization may differ between the sexes or species. This is particularly likely for reinforcement based on postmating prezygotic (PMPZ) incompatibilities, as the ability to fertilize both conspecific and heterospecific eggs is beneficial to male gametes, but heterospecific mating may incur a cost for female gametes. We develop a population genetic model of interspecific conflict over reinforcement inspired by "gametophytic factors", which act as PMPZ barriers among Zea mays subspecies. We demonstrate that this conflict results in the transient evolution of reinforcement-after females adaptively evolve to reject gametes lacking a signal common in conspecific gametes, this gamete signal adaptively introgresses into the other population. Ultimately, the male gamete signal fixes in both species, and isolation returns to pre-reinforcement levels. We interpret geographic patterns of isolation among Z. mays subspecies considering these findings and suggest when and how this conflict can be resolved. Our results suggest that sexual conflict over fertilization may pose an understudied obstacle to the evolution of reinforcement.

Analysis of ancestry heterozygosity suggests that hybrid incompatibilities in threespine stickleback are environment dependent.

Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are "intrinsic," meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F2 hybrid crosses between divergent populations of threespine stickleback fish (Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse-albeit indirect-signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities.

Early-acting inbreeding depression can evolve as an inbreeding avoidance mechanism.

Despite the potential for mechanical, developmental and/or chemical mechanisms to prevent self-fertilization, incidental self-fertilization is inevitable in many predominantly outcrossing species. In such cases, inbreeding can compromise individual fitness. Unquestionably, much of this inbreeding depression is maladaptive. However, we show that when reproductive compensation allows for the replacement of inviable embryos lost early in development, selection can favour deleterious recessive variants that induce 'self-sacrificial' death of inbred embryos. Our theoretical results provide numerous testable predictions which could challenge the assumption that inbreeding depression is always maladaptive. Our work is applicable any species that cannot fully avoid inbreeding, exhibits substantial inbreeding depression, and has the potential to compensate embryos lost early in development. In addition to its general applicability, our theory suggests that self-sacrificial variants might be responsible for the remarkably low realized selfing rates of gymnosperms with high primary selfing rates, as gymnosperms exhibit strong inbreeding depression, have effective reproductive compensation mechanisms, and cannot evolve chemical self-incompatibility.

Together inbreeding and reproductive compensation favor lethal t-haplotypes.

Male mice who are heterozygous for distorting and non-distorting alleles at the t-haplotype transmit the driving t-haplotype around 90% of the time-a drastic departure from Mendelian expectations. This selfish act comes at a cost. The mechanism underlying transmission distortion in this system causes severe sterility in males homozygous for the drive alleles, ultimately preventing its fixation. Curiously, many driving t-haplotypes also induce embryonic lethality in both sexes when homozygous; however, this is neither universal nor a necessity for this distortion mechanism. Charlesworth provided an adaptive explanation for the evolution of lethal t-haplotypes in a population segregating for distorting and non-distorting t alleles-if mothers compensate by replacing dead embryos with new offspring (or by transferring energy to surviving offspring), a recessive lethal can be favored because it effectively allows mothers the opportunity to trade in infertile males for potentially fertile offspring. This model, however, requires near complete reproductive compensation for the invasion of the lethal t-haplotype and produces an equilibrium frequency of lethal drivers well below what is observed in nature. We show that low levels of systemic inbreeding, which we model as brother-sister mating, allow lethal t-haplotypes to invade with much lower levels of reproductive compensation. Furthermore, inbreeding allows these lethal haplotypes to largely displace the ancestral male-sterile haplotypes. Our results show that together inbreeding and reproductive compensation move expected equilibria closer to observed haplotype frequencies in natural populations and occur under lower, potentially more reasonable, parameters.

Widespread imprinting of transposable elements and variable genes in the maize endosperm.

Fertilization and seed development is a critical time in the plant life cycle, and coordinated development of the embryo and endosperm are required to produce a viable seed. In the endosperm, some genes show imprinted expression where transcripts are derived primarily from one parental genome. Imprinted gene expression has been observed across many flowering plant species, though only a small proportion of genes are imprinted. Understanding how imprinted expression arises has been complicated by the reliance on single nucleotide polymorphisms between alleles to enable testing for imprinting. Here, we develop a method to use whole genome assemblies of multiple genotypes to assess for imprinting of both shared and variable portions of the genome using data from reciprocal crosses. This reveals widespread maternal expression of genes and transposable elements with presence-absence variation within maize and across species. Most maternally expressed features are expressed primarily in the endosperm, suggesting that maternal de-repression in the central cell facilitates expression. Furthermore, maternally expressed TEs are enriched for maternal expression of the nearest gene, and read alignments over maternal TE-gene pairs indicate that these are fused rather than independent transcripts.

Reproductive Compensation and Selection among Viable Embryos Drive the Evolution of Polyembryony.

AbstractSimple polyembryony, where one gametophyte produces multiple embryos with different sires but the same maternal haplotype, is common among vascular plants. We develop an infinite-sites, forward population genetics model showing that together polyembryony's two benefits-"reproductive compensation" achieved by providing a backup for inviable embryos and the opportunity to favor the fitter of surviving embryos-can favor its evolution. Our model tests how these factors can favor the evolution of polyembryony and how these underlying benefits of polyembryony shape the genetic load under a range of biological parameters. While these two benefits are difficult to disentangle in nature, we construct variant models of polyembryony that either only include or only exclude the opportunity for reproductive compensation. We find that reproductive compensation strongly favors the evolution of polyembryony and that polyembryony is favored much more weekly in its absence, suggesting that the benefit of a backup embryo is the major force favoring polyembryony. Remarkably, we find nearly identical results in cases in which mutations impact either embryonic or postembryonic fitness (no pleiotropy) and in cases in which mutations have identical effects on embryonic and postembryonic fitness (extreme pleiotropy). Finally, we find that the consequences of polyembryony depend on its function-polyembryony results in a decrease in mean embryonic fitness when acting as a mechanism of embryo compensation and ultimately increases mean embryonic fitness when we exclude this potential benefit.

Making a Murderer: The Evolutionary Framing of Hybrid Gamete-Killers.

Recent molecular investigations of hybrid incompatibilities have revealed fascinating patterns of genetic interactions that have been interpreted as the remnants of a history of selfish evolution. Instead of framing hybrid incompatibilities in light of genetic conflict, we advocate assuming their innocence. Researchers must build a strong theory for each case, supported by population genetic evidence, such that the role of conflict in the evolution of a hybrid incompatibility can be proven beyond reasonable doubt. This will require careful investigation of the evolutionary history of these incompatibilities, a reckoning of how the reproductive biology of study organisms impacts on the likelihood of genetic conflict, and molecular evidence of the rapid selfish spread of these alleles.

Development of first linkage map for Silphium integrifolium (Asteraceae) enables identification of sporophytic self-incompatibility locus.

Silphium integrifolium (Asteraceae) has been identified as a candidate for domestication as a perennial oilseed crop and is assumed to have sporophytic self-incompatibility system-the genetic basis of which is not well understood in the Asteraceae. To address this gap, we sought to map the genomic location of the self-recognition locus (S-locus) in this species. We used a biparental population and genotyping-by-sequencing to create the first genetic linkage map for this species, which contained 198 SNP markers and resolved into the correct number of linkage groups. Then we developed a novel crossing scheme and set of analysis methods in order to infer S-locus genotypes for a subset of these individuals, allowing us to map the trait. Finally, we evaluated potential genes of interest using synteny analysis with the annual sunflower (Helianthus annuus) and lettuce (Lactuca sativa) genomes. Our results confirm that S. integrifolium does indeed have a sporophytic self-incompatibility system. Our method is effective and efficient, allowed us to map the S. integrifolium S-locus using fewer resources than existing methods, and could be readily applied to other species.

Diversification or Collapse of Self-Incompatibility Haplotypes as a Rescue Process.

AbstractIn angiosperm self-incompatibility systems, pollen with an allele matching the pollen recipient at the self-incompatibility locus is rejected. Extreme allelic polymorphism is maintained by frequency-dependent selection favoring rare alleles. However, two challenges result in a chicken-or-egg problem for the spread of a new allele (a tightly linked haplotype in this case) under the widespread "collaborative non-self-recognition" mechanism. A novel pollen function mutation alone would merely grant compatibility with a nonexistent style function allele: a neutral change at best. A novel pistil function mutation alone could be fertilized only by pollen with a nonexistent pollen function allele: a deleterious change that would reduce seed set to zero. However, a pistil function mutation complementary to a previously neutral pollen mutation may spread if it restores self-incompatibility to a self-compatible intermediate. We show that novel haplotypes can also drive elimination of existing ones with fewer siring opportunities. We calculate relative probabilities of increase and collapse in haplotype number given the initial collection of incompatibility haplotypes and the population gene conversion rate. Expansion in haplotype number is possible when population gene conversion rate is large, but large contractions are likely otherwise. A Markov chain model derived from these expansion and collapse probabilities generates a stable haplotype number distribution in the realistic range of 10-40 under plausible parameters. However, smaller populations might lose many haplotypes beyond those lost by chance during bottlenecks.

Non-self recognition-based self-incompatibility can alternatively promote or prevent introgression.

Self-incompatibility alleles (S-alleles), which prevent self-fertilisation in plants, have historically been expected to benefit from negative frequency-dependent selection and invade when introduced to a new population through gene flow. However, the most taxonomically widespread form of self-incompatibility, the ribonuclease-based system ancestral to the core eudicots, functions through collaborative non-self recognition, which can affect both short-term patterns of gene flow and the long-term process of S-allele diversification. We analysed a model of S-allele evolution in two populations connected by migration, focussing on comparisons among the fates of S-alleles initially unique to each population and those shared among populations. We found that both shared and unique S-alleles from the population with more unique S-alleles were usually fitter compared with S-alleles from the population with fewer S-alleles. Resident S-alleles often became extinct and were replaced by migrant S-alleles, although this outcome could be averted by pollen limitation or biased migration. Collaborative non-self recognition will usually either result in the whole-sale replacement of S-alleles from one population with those from another or else disfavour introgression of S-alleles altogether.

Measurements of lethal and nonlethal inbreeding depression inform the de novo domestication of Silphium integrifolium.

PREMISE: Inbreeding depression, or the reduction in fitness of progeny with related parents, has the potential to adversely affect the long-term viability of both wild and captive plant populations. Silphium integrifolium, a prairie plant native to the central United States, has been identified as a potential candidate for domestication as a perennial oilseed crop. Little is known about the potential for inbreeding depression in this species, but it is expected to be nonnegligible because S. integrifolium is both perennial and self-incompatible. Here, we measure lethal inbreeding depression expressed through embryo deaths, and nonlethal inbreeding depression expressed through changes in vigor and fitness phenotypes of progeny. METHODS: First, we made controlled crosses among related and unrelated individuals to determine the effect of two different levels of inbreeding on seed production. Then, we grew inbred and outbred progeny from this population to reproductive maturity and measured 11 key traits. RESULTS: We found that within an improved S. integrifolium population, individuals carried an average of slightly less than one lethal allele per gamete. In progeny, significant inbreeding depression was observed in at least one family for eight of the 11 measured traits. CONCLUSIONS: Inbreeding depression is likely to be an important challenge to S. integrifolium domestication, reducing overall population fecundity and values for important phenotypes. These effects may grow worse as selection reduces effective population size. We recommend several strategies for S. integrifolium breeding to help mitigate these problems.

Patterns of genetic variation in a prairie wildflower, Silphium integrifolium, suggest a non-prairie origin and locally adaptive variation.

PREMISE: Understanding the relationship between genetic structure and geography provides information about a species' history and can be used for breeding and conservation goals. The North American prairie is interesting because of its recent origin and subsequent fragmentation. Silphium integrifolium, an iconic perennial American prairie wildflower, is targeted for domestication, having undergone a few generations of improvement. We present the first application of population genetic data in this species to address the following goals: (1) improve breeding by characterizing genetic structure and (2) identify the species geographic origin and potential targets and drivers of selection during range expansion. METHODS: We developed a reference transcriptome as a genotyping reference for samples from throughout the species range. Population genetic analyses were used to describe patterns of genetic variation, and demographic modeling was used to characterize potential processes that shaped variation. Outlier scans for selection and associations with environmental variables were used to identify loci linked to putative targets and drivers of selection. RESULTS: Genetic variation partitioned samples into three geographic clusters. Patterns of variation and demographic modeling suggest that the species origin is in the American Southeast. Breeding program accessions are from the region with lowest observed genetic variation. CONCLUSIONS: This prairie species did not originate within the prairie. Breeding may be improved by including accessions from outside of the germplasm founding region. The geographic structuring and the identified targets and drivers of adaptation can guide collecting efforts toward populations with beneficial agronomic traits.

The Unreasonable Effectiveness of Convolutional Neural Networks in Population Genetic Inference.

Population-scale genomic data sets have given researchers incredible amounts of information from which to infer evolutionary histories. Concomitant with this flood of data, theoretical and methodological advances have sought to extract information from genomic sequences to infer demographic events such as population size changes and gene flow among closely related populations/species, construct recombination maps, and uncover loci underlying recent adaptation. To date, most methods make use of only one or a few summaries of the input sequences and therefore ignore potentially useful information encoded in the data. The most sophisticated of these approaches involve likelihood calculations, which require theoretical advances for each new problem, and often focus on a single aspect of the data (e.g., only allele frequency information) in the interest of mathematical and computational tractability. Directly interrogating the entirety of the input sequence data in a likelihood-free manner would thus offer a fruitful alternative. Here, we accomplish this by representing DNA sequence alignments as images and using a class of deep learning methods called convolutional neural networks (CNNs) to make population genetic inferences from these images. We apply CNNs to a number of evolutionary questions and find that they frequently match or exceed the accuracy of current methods. Importantly, we show that CNNs perform accurate evolutionary model selection and parameter estimation, even on problems that have not received detailed theoretical treatments. Thus, when applied to population genetic alignments, CNNs are capable of outperforming expert-derived statistical methods and offer a new path forward in cases where no likelihood approach exists.

The effect of autopolyploidy on population genetic signals of hard sweeps.

Searching for population genomic signals left behind by positive selection is a major focus of evolutionary biology, particularly as sequencing technologies develop and costs decline. The effect of the number of chromosome copies (i.e. ploidy) on the manifestation of these signals remains an outstanding question, despite a wide appreciation of ploidy being a fundamental parameter governing numerous biological processes. We clarify the principal forces governing the differential manifestation and persistence of the selection signal by separating the effects of polyploidy on the rates of fixation versus rates of diversity (i.e. mutation and recombination) using coalescent simulations. We explore the major consequences of polyploidy, finding a more localized signal, greater dependence on dominance and longer persistence of the signal following fixation, and discuss what this means for within- and across ploidy inference on the strength and prevalence of selective sweeps. As genomic advances continue to open doors for interrogating natural systems, simulations such as this aid our ability to interpret and compare data across ploidy levels.

The Limits of Natural Selection in a Nonequilibrium World.

Evolutionary theory predicts that factors such as a small population size or low recombination rate can limit the action of natural selection. The emerging field of comparative population genomics offers an opportunity to evaluate these hypotheses. However, classical theoretical predictions assume that populations are at demographic equilibrium. This assumption is likely to be violated in the very populations researchers use to evaluate selection's limits: populations that have experienced a recent shift in population size and/or effective recombination rates. Here we highlight theory and data analyses concerning limitations on the action of natural selection in nonequilibrial populations and argue that substantial care is needed to appropriately test whether species and populations show meaningful differences in selection efficacy. A move toward model-based inferences that explicitly incorporate nonequilibrium dynamics provides a promising approach to more accurately contrast selection efficacy across populations and interpret its significance.

Mating system variation in hybrid zones: facilitation, barriers and asymmetries to gene flow.

Plant mating systems play a key role in structuring genetic variation both within and between species. In hybrid zones, the outcomes and dynamics of hybridization are usually interpreted as the balance between gene flow and selection against hybrids. Yet, mating systems can introduce selective forces that alter these expectations; with diverse outcomes for the level and direction of gene flow depending on variation in outcrossing and whether the mating systems of the species pair are the same or divergent. We present a survey of hybridization in 133 species pairs from 41 plant families and examine how patterns of hybridization vary with mating system. We examine if hybrid zone mode, level of gene flow, asymmetries in gene flow and the frequency of reproductive isolating barriers vary in relation to mating system/s of the species pair. We combine these results with a simulation model and examples from the literature to address two general themes: (1) the two-way interaction between introgression and the evolution of reproductive systems, and (2) how mating system can facilitate or restrict interspecific gene flow. We conclude that examining mating system with hybridization provides unique opportunities to understand divergence and the processes underlying reproductive isolation.

The evolutionary response of mating system to heterosis.

Isolation allows populations to diverge and to fix different alleles. Deleterious alleles that reach locally high frequencies contribute to genetic load, especially in inbred or selfing populations, in which selection is relaxed. In the event of secondary contact, the recessive portion of the genetic load is masked in the hybrid offspring, producing heterosis. This advantage, only attainable through outcrossing, should favour evolution of greater outcrossing even if inbreeding depression has been purged from the contributing populations. Why, then, are selfing-to-outcrossing transitions not more common? To evaluate the evolutionary response of mating system to heterosis, we model two monomorphic populations of entirely selfing individuals, introduce a modifier allele that increases the rate of outcrossing and investigate whether the heterosis among populations is sufficient for the modifier to invade and fix. We find that the outcrossing mutation invades for many parameter choices, but it rarely fixes unless populations harbour extremely large unique fixed genetic loads. Reversions to outcrossing become more likely as the load becomes more polygenic, or when the modifier appears on a rare background, such as by dispersal of an outcrossing genotype into a selfing population. More often, the outcrossing mutation instead rises to moderate frequency, which allows recombination in hybrids to produce superior haplotypes that can spread without the mutation's further assistance. The transience of heterosis can therefore explain why secondary contact does not commonly yield selfing-to-outcrossing transitions.