Massive haplotypes underlie ecotypic differentiation in sunflowers.

Species often include multiple ecotypes that are adapted to different environments1. However, it is unclear how ecotypes arise and how their distinctive combinations of adaptive alleles are maintained despite hybridization with non-adapted populations2-4. Here, by resequencing 1,506 wild sunflowers from 3 species (Helianthus annuus, Helianthus petiolaris and Helianthus argophyllus), we identify 37 large (1-100 Mbp in size), non-recombining haplotype blocks that are associated with numerous ecologically relevant traits, as well as soil and climate characteristics. Limited recombination in these haplotype blocks keeps adaptive alleles together, and these regions differentiate sunflower ecotypes. For example, haplotype blocks control a 77-day difference in flowering between ecotypes of the silverleaf sunflower H. argophyllus (probably through deletion of a homologue of FLOWERING LOCUS T (FT)), and are associated with seed size, flowering time and soil fertility in dune-adapted sunflowers. These haplotypes are highly divergent, frequently associated with structural variants and often appear to represent introgressions from other-possibly now-extinct-congeners. These results highlight a pervasive role of structural variation in ecotypic adaptation.

Evolutionary dynamics of recent selection on cognitive abilities.

Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper wasp Polistes fuscatus-a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps in P. fuscatus contain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures in P. fuscatus' recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves.

The effect of leaf shape on the thermoregulation and frost tolerance of an annual vine, Ipomoea hederacea (Convolvulaceae).

PREMISE OF STUDY: Leaf shape is predicted to have important ecophysiological consequences; for example, theory predicts that lobed leaves should track air temperature more closely than their entire-margined counterparts. Hence, leaf-lobing may be advantageous during cold nights (∼0°C) when there is the risk of damage by radiation frost (a phenomenon whereby leaves fall below air temperature because of an imbalance between radiational heat loss and convective heat gain). METHODS: Here, we test whether radiation frost can lead to differential damage between leaf shapes by examining a leaf-shape polymorphism in Ipomoea hederacea, where leaves are either lobed or heart-shaped depending on a single Mendelian locus. We logged leaf temperature during midautumn, and measured chlorophyll fluorescence and survival as proxies of performance. Furthermore, we tested if the leaf-shape locus confers freezing tolerance using freezing assays on leaf tissue from different leaf shapes. KEY RESULTS: We found that lobed leaves consistently remain warmer than heart-shaped leaves during the night, but that no pattern emerged during the day, and that temperature differences between leaf shapes were typically small. Furthermore, we found that leaf types did not differ in frost tolerance, but that a 1°C decrease leads to a transition from moderate to complete damage. CONCLUSIONS: Our results demonstrate that Ipomoea hederacea leaf shapes do experience different nighttime temperatures, and that only minor temperature differences can lead to disparate levels of freezing damage, suggesting that the differential thermoregulation could result in different levels of frost damage.

Adaptation with gene flow across the landscape in a dune sunflower.

Isolation by adaptation increases divergence at neutral loci when natural selection against immigrants reduces the rate of gene flow between different habitats. This can occur early in the process of adaptive divergence and is a key feature of ecological speciation. Despite the ability of isolation by distance (IBD) and other forms of landscape resistance to produce similar patterns of neutral divergence within species, few studies have used landscape genetics to control for these other forces. We have studied the divergence of Helianthus petiolaris ecotypes living in active sand dunes and adjacent non-dune habitat, using landscape genetics approaches, such as circuit theory and multiple regression of distance matrices, in addition to coalescent modelling. Divergence between habitats was significant, but not strong, and was shaped by IBD. We expected that increased resistance owing to patchy and unfavourable habitat in the dunes would contribute to divergence. Instead, we found that landscape resistance models with lower resistance in the dunes performed well as predictors of genetic distances among subpopulations. Nevertheless, habitat class remained a strong predictor of genetic distance when controlling for isolation by resistance and IBD. We also measured environmental variables at each site and confirmed that specific variables, especially soil nitrogen and vegetation cover, explained a greater proportion of variance in genetic distance than did landscape or the habitat classification alone. Asymmetry in effective population sizes and numbers of migrants per generation was detected using coalescent modelling with Bayesian inference, which is consistent with incipient ecological speciation being driven by the dune habitat.

Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance.

Domesticated plants and animals often display dramatic responses to selection, but the origins of the genetic diversity underlying these responses remain poorly understood. Despite domestication and improvement bottlenecks, the cultivated sunflower remains highly variable genetically, possibly due to hybridization with wild relatives. To characterize genetic diversity in the sunflower and to quantify contributions from wild relatives, we sequenced 287 cultivated lines, 17 Native American landraces and 189 wild accessions representing 11 compatible wild species. Cultivar sequences failing to map to the sunflower reference were assembled de novo for each genotype to determine the gene repertoire, or 'pan-genome', of the cultivated sunflower. Assembled genes were then compared to the wild species to estimate origins. Results indicate that the cultivated sunflower pan-genome comprises 61,205 genes, of which 27% vary across genotypes. Approximately 10% of the cultivated sunflower pan-genome is derived through introgression from wild sunflower species, and 1.5% of genes originated solely through introgression. Gene ontology functional analyses further indicate that genes associated with biotic resistance are over-represented among introgressed regions, an observation consistent with breeding records. Analyses of allelic variation associated with downy mildew resistance provide an example in which such introgressions have contributed to resistance to a globally challenging disease.

Multiple reproductive barriers separate recently diverged sunflower ecotypes.

Measuring reproductive barriers between groups of organisms is an effective way to determine the traits and mechanisms that impede gene flow. However, to understand the ecological and evolutionary factors that drive speciation, it is important to distinguish between the barriers that arise early in the speciation process and those that arise after speciation is largely complete. In this article, we comprehensively test for reproductive isolation between recently diverged (<10,000 years bp) dune and nondune ecotypes of the prairie sunflower, Helianthus petiolaris. We find reproductive barriers acting at multiple stages of hybridization, including premating, postmating-prezygotic, and postzygotic barriers, despite the recent divergence. Barriers include extrinsic selection against immigrants and hybrids, a shift in pollinator assemblage, and postpollination assortative mating. Together, these data suggest that multiple barriers can be important for reducing gene flow in the earliest stages of speciation.

Hybridization and extinction.

Hybridization may drive rare taxa to extinction through genetic swamping, where the rare form is replaced by hybrids, or by demographic swamping, where population growth rates are reduced due to the wasteful production of maladaptive hybrids. Conversely, hybridization may rescue the viability of small, inbred populations. Understanding the factors that contribute to destructive versus constructive outcomes of hybridization is key to managing conservation concerns. Here, we survey the literature for studies of hybridization and extinction to identify the ecological, evolutionary, and genetic factors that critically affect extinction risk through hybridization. We find that while extinction risk is highly situation dependent, genetic swamping is much more frequent than demographic swamping. In addition, human involvement is associated with increased risk and high reproductive isolation with reduced risk. Although climate change is predicted to increase the risk of hybridization-induced extinction, we find little empirical support for this prediction. Similarly, theoretical and experimental studies imply that genetic rescue through hybridization may be equally or more probable than demographic swamping, but our literature survey failed to support this claim. We conclude that halting the introduction of hybridization-prone exotics and restoring mature and diverse habitats that are resistant to hybrid establishment should be management priorities.

Establishing genomic tools and resources for Guizotia abyssinica (L.f.) Cass.-the development of a library of expressed sequence tags, microsatellite loci, and the sequencing of its chloroplast genome.

We present an EST library, chloroplast genome sequence, and nuclear microsatellite markers that were developed for the semi-domesticated oilseed crop noug (Guizotia abyssinica) from Ethiopia. The EST library consists of 25 711 Sanger reads, assembled into 17 538 contigs and singletons, of which 4781 were functionally annotated using the Arabidopsis Information Resource (TAIR). The age distribution of duplicated genes in the EST library shows evidence of two paleopolyploidizations-a pattern that noug shares with several other species in the Heliantheae tribe (Compositae family). From the EST library, we selected 43 microsatellites and then designed and tested primers for their amplification. The number of microsatellite alleles varied between 2 and 10 (average 4.67), and the average observed and expected heterozygosities were 0.49 and 0.54, respectively. The chloroplast genome was sequenced de novo using Illumina's sequencing technology and completed with traditional Sanger sequencing. No large re-arrangements were found between the noug and sunflower chloroplast genomes, but 1.4% of sites have indels and 1.8% show sequence divergence between the two species. We identified 34 tRNAs, 4 rRNA sequences, and 80 coding sequences, including one region (trnH-psbA) with 15% sequence divergence between noug and sunflower that may be particularly useful for phylogeographic studies in noug and its wild relatives.