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Papa, R.

Publications and source records attributed to Papa, R..

30 records · Page 2Linked to original sources

The genomic signature of wild-to-crop introgression during the domestication of scarlet runner bean (Phaseolus coccineus L.)

O_LIThe scarlet runner bean is an open-pollinated legume from the highlands of Mesoamerica that is cultivated in small-scale agriculture for its dry seeds and immature pods. Demographic bottlenecks associated with domestication might reduce genetic diversity and facilitate the accumulation of deleterious mutations. Conversely, introgression from wild relatives could be a source of variation. C_LIO_LIUsing Genotyping by Sequencing data (79,286 SNVs) from 237 cultivated and wild samples, we evaluated the demographic history of traditional varieties from different regions of Mexico and looked for evidence of introgression between sympatric wild and cultivated populations. C_LIO_LITraditional varieties have high levels of diversity, even though there is evidence of a severe initial genetic bottleneck, followed by a population expansion. Introgression from wild to domesticated populations was detected, but not in the opposite direction. This asymmetric introgression might contribute to the recovery of genetic variation and it has occurred at different times: constantly in the center of Mexico; recently in the North West; and anciently in the South. C_LIO_LISeveral factors are acting together to increase and maintain genetic diversity in P. coccineus cultivars, such as demographic expansion and introgression. Wild relatives represent a valuable genetic resource and have played a key role in scarlet runner bean evolution via introgression into traditional varieties. C_LI

evolutionary biology↗

Selection and gene flow define polygenic barriers between incipient butterfly species

Characterizing the genetic architecture of species boundaries remains a difficult task. Hybridizing species provide a powerful system to identify the factors that shape genomic variation and, ultimately, identify the regions of the genome that maintain species boundaries. Unfortunately, complex histories of isolation, admixture and selection can generate heterogenous genomic landscapes of divergence which make inferences about the regions that are responsible for species boundaries problematic. However, as the signal of admixture and selection on genomic loci varies with recombination rate, their relationship can be used to infer their relative importance during speciation. Here, we explore patterns of genomic divergence, admixture and recombination rate among hybridizing lineages across the Heliconius erato radiation. We focus on the incipient species, H. erato and H. himera, and distinguish the processes that drive genomic divergence across three contact zones where they frequently hybridize. Using demographic modeling and simulations, we infer that periods of isolation and selection have been major causes of genome-wide correlation patterns between recombination rate and divergence between these incipient species. Upon secondary contact, we found surprisingly highly asymmetrical introgression between the species pair, with a paucity of H. erato alleles introgressing into the H. himera genomes. We suggest that this signal may result from a current polygenic species boundary between the hybridizing lineages. These results contribute to a growing appreciation for the importance of polygenic architectures of species boundaries and pervasive genome-wide selection during the early stages of speciation with gene flow.

evolutionary biology↗

Pod indehiscence in common bean is associated to the fine regulation of PvMYB26 and a non-functional abscission layer

In legumes, pod shattering occurs when mature pods dehisce along the sutures, and detachment of the valves promotes seed dispersal. In Phaseolus vulgaris, the major locus qPD5.1-Pv for pod indehiscence was identified recently. We developed a BC4/F4 introgression line population and narrowed the major locus down to a 22.5-kb region. Here, gene expression and a parallel histological analysis of dehiscent and indehiscent pods identified an AtMYB26 orthologue as the best candidate for loss of pod shattering, on a genomic region ~11 kb downstream of the highest associated peak. Based on mapping and expression data, we propose early and fine up-regulation of PvMYB26 in dehiscent pods. Detailed histological analysis establishes that pod indehiscence is associated to the lack of a functional abscission layer in the ventral sheath, and that the key anatomical modifications associated with pod shattering in common bean occur early during pod development. We finally propose that loss of pod shattering in legumes resulted from histological convergent evolution and that this is the result of selection at orthologous loci. One-sentence summaryA non-functional abscission layer determines the loss of pod shattering; mapping data, and parallel gene expression and histological analysis support PvMYB26 as the candidate gene for pod indehiscence.

genetics↗

Neural processing genes are linked to divergence in visual mate preference in sympatric Heliconius butterflies

Many animal species remain separate not because they fail to produce viable hybrids, but because their individuals choose not to mate. However, we still know very little of the genetic mechanisms underlying changes in these mate preference behaviours. Heliconius butterflies display bright warning patterns, which they also use to recognize conspecifics. Here, we couple QTL for divergence in visual preference behaviours with population genomic and gene expression analyses of neural tissue (central brain, optic lobes and ommatidia) across development in two sympatric Heliconius species. Within a region containing 200 genes, we identify five genes that are strongly associated with divergent visual preferences. Three of these have previously been implicated in key components of neural signalling (specifically an ionotropic glutamate receptor and two regucalcins), and overall our candidates suggest shifts in behaviour involve changes in visual integration or processing. This would allow preference evolution without altering perception of the wider environment.

evolutionary biology↗

Comparative analysis based on transcriptomics and metabolomics data reveal differences between emmer and durum wheat in response to nitrogen starvation

Mounting evidence indicates the key role of Nitrogen (N) on diverse processes in plant, including not only yield but also development and defense. Using a combined transcriptomics and metabolomics approach, we studied the response of seedlings to N starvation of two different tetraploid wheat genotypes from the two main domesticated subspecies, emmer (Triticum turgidum ssp. dicoccum) and durum wheat (Triticum turgidum ssp. durum). We found that durum wheat exhibits broader and stronger response in comparison to emmer as evidenced by the analysis of the differential expression pattern of both genes and metabolites and gene enrichment analysis. Emmer and durum wheat showed major differences in the responses to N starvation for transcription factor families. While emmer showed differential reduction in the levels of primary metabolites to N starvation, durum wheat exhibited increased levels of most metabolites, including GABA as an indicator of metabolic imbalance. The correlation-based networks including the differentially expressed genes and metabolites revealed tighter regulation of metabolism in durum wheat in comparison to emmer, as evidenced by the larger number of significant correlations. We also found that glutamate and GABA had highest values of centrality in the metabolic correlation network, suggesting their critical role in the genotype-specific response to N starvation of emmer and durum wheat, respectively. Moreover, this finding indicates that there might be contrasting strategies associated to GABA and Glutamate signaling modulating shoot vs root growth in the two different wheat subspecies.

plant biology↗

Perfect mimicry between Heliconius butterflies is constrained by genetics and development

Mullerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. The butterfly species Heliconius erato and Heliconius melpomene have a large diversity of co-mimicking geographic races with remarkable resemblance in melanic patterning across the mid-forewing that has been linked to expression patterns of the gene WntA. Recent CRISPR/Cas9 experiments have informed us on the exact areas of the wings in which WntA affects color pattern formation in both H. erato and H. melpomene, thus providing a unique comparative dataset to explore the functioning of a gene and its potential effect on phenotypic evolution. We therefore quantified wing color pattern differences in the mid-forewing region of 14 co-mimetic races of H. erato and H. melpomene and measured the extent to which mimicking races are not perfectly identical. While the relative size of the mid-forewing pattern is generally nearly identical, our results highlight the areas of the wing that prevent these species from achieving perfect mimicry and demonstrate that this mismatch can be largely explained by constraints imposed by divergence in the gene regulatory network that define wing color patterning. Divergence in the developmental architecture of a trait can thus constrain morphological evolution even between relatively closely related species.

evolutionary biology↗

Ancient genomes reveal early Andean farmers selected common beans while preserving diversity

All crops are the product of a domestication process that started less than 12,000 years ago from one or more wild populations [1, 2]. Farmers selected desirable phenotypic traits, such as improved energy accumulation, palatability of seeds or reduced natural shattering [3], while leading domesticated populations through several more or less gradual demographic contractions [2, 4]. As a consequence, erosion of wild genetic variation [5] is typical of modern cultivars making them highly susceptible to pathogens, pests and environmental change [6,7]. The loss of genetic diversity hampers further crop improvement programs to increase food production in a changing world, posing serious threats to food security [8,9]. Using both ancient and modern seeds, we analyzed the temporal dynamic of genetic variation and selection during the domestication process of the common bean (Phaseolus vulgaris) that occurred in the Southern Andes. Here we show that most domestic traits were selected for prior to 2,500 years ago, with no or only minor loss of whole-genome variation. In fact, i) all ancient domestic genomes dated between 600 and 2,500 years ago are highly variable - at least as variable as a modern genome from the wild; the genetic erosion that we observe in modern cultivars is therefore a recent process that occurred in the last centuries; ii) the majority of changes at coding genes that differentiate wild and domestic genomes are already present in the ancient genomes analyzed here. Considering that most desirable phenotypic traits are likely controlled by multiple polymorphic genes [10], a likely explanation of this decoupling of selection and genomic erosion is that early farmers applied a relatively weak selection pressure [2] by using many phenotypically similar but genomically diverse individuals as breeders. Selection strategies during the last few centuries were probably less sustainable and produced further improvements focusing on few plants carrying the traits of interest, at the cost of marked genetic erosion.

genomics↗

Multiple loci control eyespot number variation on the hindwings of Bicyclus anynana butterflies

The underlying genetic changes that regulate the appearance and disappearance of repeated traits, or serial homologs, remain poorly understood. One hypothesis is that variation in genomic regions flanking master regulatory genes, also known as input-output genes, controls variation in trait number, making the locus of evolution almost predictable. Other hypotheses implicate genetic variation in up-stream or downstream loci of master control genes. Here, we use the butterfly Bicyclus anynana, a species which exhibits natural variation in eyespot number on the dorsal hindwing, to test these two hypotheses. We first estimated the heritability of dorsal hindwing eyespot number by breeding multiple butterfly families differing in eyespot number, and regressing eyespot number of offspring on mid-parent values. We then estimated the number and identity of independent genetic loci contributing to eyespot number variation by performing a genome-wide association study with restriction site-associated DNA Sequencing (RAD-seq) from multiple individuals varying in number of eyespots sampled across a freely breeding lab population. We found that dorsal hindwing eyespot number has a moderately high heritability of approximately 0.50. In addition, multiple loci near previously identified genes involved in eyespot development display high association with dorsal hindwing eyespot number, suggesting that homolog number variation is likely determined by regulatory changes at multiple loci that build the trait and not by variation at single master regulators or input-output genes.\n\nData accessibilityThe Bicyclus anynana PstI RAD-tag sequencing data is available via the Genbank BioProject PRJNA509697. Genotype VCF files will be made available through Figshare upon acceptance.

genetics↗

The genetic basis of hindwing eyespot number variation in Bicyclus anynana butterflies

The underlying genetic changes that regulate the appearance and disappearance of repeated traits, or serial homologs, remain poorly understood. One hypothesis is that variation in genomic regions flanking master regulatory genes, also known as input-output genes, controls variation in trait number, making the locus of evolution almost predictable. Other hypotheses implicate genetic variation in up-stream or downstream loci of master control genes. Here, we use the butterfly Bicyclus anynana, a species which exhibits natural variation in eyespot number on the dorsal hindwing, to test these two hypotheses. We first estimated the heritability of dorsal hindwing eyespot number by breeding multiple butterfly families differing in eyespot number, and regressing eyespot number of offspring on mid-parent values. We then estimated the number and identity of independent genetic loci contributing to eyespot number variation by performing a genome-wide association study with restriction site-associated DNA Sequencing (RAD-seq) from multiple individuals varying in number of eyespots sampled across a freely breeding lab population. We found that dorsal hindwing eyespot number has a moderately high heritability of approximately 0.50. In addition, multiple loci near previously identified genes involved in eyespot development display high association with dorsal hindwing eyespot number, suggesting that homolog number variation is likely determined by regulatory changes at multiple loci that build the trait and not by variation at single master regulators or input-output genes.

genetics↗

Genomic architecture and introgression shape a butterfly radiation

We here pioneer a low-cost assembly strategy for 20 Heliconiini genomes to characterize the evolutionary history of the rapidly radiating genus Heliconius. A bifurcating tree provides a poor fit to the data, and we therefore explore a reticulate phylogeny for Heliconius. We probe the genomic architecture of gene flow, and develop a new method to distinguish incomplete lineage sorting from introgression. We find that most loci with non-canonical histories arose through introgression, and are strongly underrepresented in regions of low recombination and high gene density. This is expected if introgressed alleles are more likely to be purged in such regions due to tighter linkage with incompatibility loci. Finally, we identify a hitherto unrecognized inversion, and show it is a convergent structural rearrangement that captures a known color pattern switch locus within the genus. Our multi-genome assembly approach enables an improved understanding of adaptive radiation.

evolutionary biology↗

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a large-X effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, i.e. faster-X, or barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply post-zygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of species incompatibilities. Our work demonstrates the importance of constructing an appropriate demographic null model in order to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

evolutionary biology↗

Patternize: An R Package For Quantifying Color Pattern Variation

O_LIThe use of image data to quantify, study and compare variation in the colors and patterns of organisms requires the alignment of images to establish homology, followed by color-based segmentation of images. Here we describe an R package for image alignment and segmentation that has applications to quantify color patterns in a wide range of organisms.\nC_LIO_LIpatternize is an R package that quantifies variation in color patterns obtained from image data. patternize first defines homology between pattern positions across specimens either through manually placed homologous landmarks or automated image registration. Pattern identification is performed by categorizing the distribution of colors using an RGB threshold, k-means clustering or watershed transformation.\nC_LIO_LIWe demonstrate that patternize can be used for quantification of the color patterns in a variety of organisms by analyzing image data for butterflies, guppies, spiders and salamanders. Image data can be compared between sets of specimens, visualized as heatmaps and analyzed using principal component analysis (PCA).\nC_LIO_LIpatternize has potential applications for fine scale quantification of color pattern phenotypes in population comparisons, genetic association studies and investigating the basis of color pattern variation across a wide range of organisms.\nC_LI

bioinformatics↗