bioRxiv Science⌕ Search

Biology subjects

Shipilina, D.

Publications and source records attributed to Shipilina, D..

9 recordsLinked to original sources

Contrasting modes of dosage compensation on ancestral and neo-Z chromosomes in butterflies

The evolution of sex chromosomes from homologous autosomes generally causes degeneration of the sex-limited chromosome (Y in XY systems and W in ZW systems), leading to altered or disrupted gene regulation. Dosage compensation has evolved repeatedly to mitigate the effects of such unbalanced expression of sex-linked genes. Previous analyses show that X chromosomes often are upregulated in males in XY-systems, while upregulation of the Z chromosome in females is unusual in ZW-systems, but understanding the generality of this pattern requires broader taxonomic sampling. In addition, little is known about how dosage compensation is established when sex chromosomes initially evolve. Here, we narrow this knowledge gap by characterizing dosage compensation in butterflies (Leptidea sp.) that harbor both ancestral, intermediate and recently derived sex chromosomes. Analyses of 120 samples, representing both sexes, different tissues and developmental stages, reveal a mixture of gene expression patterns. We confirm that downregulation in males is the predominant mode on the ancestral Z chromosome, but we find complex patterns of male downregulation and female upregulation for Z chromosomes with different evolutionary histories, as well as between different tissues. Dosage compensation has for example evolved rapidly in regions of the youngest neo-Z where the neo-W gametologs have lost function, but not in regions with functional gene copies on both Z and W. Our results provide novel insights into the complex evolutionary trajectories underlying dosage compensation and show that development of specific mechanisms likely depends on both sex chromosome system and dosage sensitivity of sex chromosome-linked genes.

evolutionary biology↗

Genealogical analysis of replicate flower colour hybrid zones in Antirrhinum

A major goal of speciation research is identifying loci that underpin barriers to gene flow. Population genomics takes a bottom-up approach, scanning the genome for molecular signatures of processes that drive or maintain divergence. However, interpreting the genomic landscape of speciation is complicated, because genome scans conflate multiple processes, most of which are not informative about gene flow. However, studying replicated population contrasts, including multiple incidences of secondary contact, can strengthen inferences. In this paper, we use linked-read sequencing (haplotagging), FST scans, and genealogical methods to characterise the genomic landscape associated with replicate hybrid zone formation. We studied two flower colour varieties of the common snapdragon, Antirrhinum majus subspecies majus, that form secondary hybrid zones in multiple independent valleys in the Pyrenees. Consistent with past work, we found very low differentiation at one well-studied zone (Planoles). However, at a second zone (Avallenet), we found stronger differentiation and greater heterogeneity, which we argue is due to differences in the amount of introgression following secondary contact. Topology weighting of genealogical trees identified loci where haplotype diversity was associated with the two snapdragon varieties. Two of the strongest associations were at previously identified flower colour loci: Flavia, that affects yellow pigmentation, and Rosea/Eluta, two linked loci that affect magenta pigmentation. Preliminary analysis of coalescence times provides additional evidence for selective sweeps at these loci and barriers to gene flow. Our study highlights the impact of demographic history on the differentiation landscape, emphasizing the need to distinguish between historical divergence and recent introgression.

evolutionary biology↗

Genome-wide cline analysis identifies new locus contributing to a barrier to gene flow across an Antirrhinum hybrid zone

Identification of the genomic regions that contribute to reproductive isolation and how they interact is a major goal of evolutionary genetics. Much effort has focused on locating candidate genes and potential barrier loci by scanning genomes for regions of excess differentiation (FST). An alternative, and perhaps more robust approach, would be to scan for genomic regions exhibiting steep clines in allele frequency across a hybrid zone. Here we develop this approach and apply it to genomic data from across a hybrid zone between varieties of Antirrhinum majus subspecies majus with different flower colour patterns (A. m. m var. pseudomajus and A. m. m var. striatum). Most steep clines are clustered in seven genomic regions, only four of which were present from FST scans between all pair-wise comparisons. Six of these regions carry previously identified loci that influence flower colour in the hybrid zone. The seventh region harbours a novel locus, RUBIA, modifying magenta intensity. Clines at RUBIA approached towards fixation on magenta side of the hybrid zone, whilst remaining polymorphic on the yellow side. This polymorphism on the yellow side may reflect a smaller phenotypic effect of RUBIA in yellow compared to magenta genetic backgrounds. Our findings illustrate how whole-genome cline scans in hybrid zones can robustly detect genomic regions contributing to phenotypic differences and highlight how different reproductive barrier loci interact across the genome.

evolutionary biology↗

Gene expression responses to environmental cues shed light on components of the migratory syndrome in butterflies

Migration is a complex behavior involving the synchronisation of many physiological and behavioral processes. Environmental cues must thus be interpreted to make decisions regarding resource allocation between, for example, migration or reproduction. In butterflies, the lack of host plants to sustain a new generation may indicate the need to migrate. Here, we used the painted lady butterfly (Vanessa cardui) as a model to characterize gene expression variation in response to host plant availability. Assessment of the response to host plant availability in adult female butterflies revealed significant modifications in gene expression, particularly within hormonal pathways (ecdysone oxidase and juvenile hormone esterase). We therefore hypothesize that tuning the ecdysone pathway may play a crucial role in regulating the timing of migration and reproduction in adult female painted lady butterflies. In addition, our analysis revealed significant enrichment of genes associated with lipid, carbohydrate, and vitamin biosynthesis, as well as the immune response. As environmental acquisition occurs throughout the life cycle, we also tracked gene expression responses to two other environmental cues across major developmental stages. Differences in both larval crowding and host plant availability during development resulted in significant changes in the expression of genes involved in development, reproduction and metabolism, particularly at the instar V larval stage. In summary, our results offer novel insights into how environmental cues affect expression profiles in migratory insects and highlight candidate genes that may underpin the migratory syndrome in the painted lady butterfly.

evolutionary biology↗

Intercontinental panmixia despite distinct migration distances in the trans-Saharan butterfly migrant Vanessa cardui

The painted lady butterfly Vanessa cardui is renowned for its virtually cosmopolitan distribution and the remarkable long-distance migrations that are part of its annual, multi-generational migratory cycle. Recently, V. cardui individuals were found north and south of the Sahara in the autumn, suggesting distinct migratory behaviours within the species. However, the evolutionary and ecological factors shaping these differences in migratory behaviour remain largely unexplored. Here, we performed whole-genome resequencing and analysed the hydrogen and strontium isotopes of 40 V. cardui individuals simultaneously collected in the autumn from regions both north and south of the Sahara. Our investigation revealed two main migratory groups: (i) short-distance migrants, journeying from temperate Europe to the circum-Mediterranean region and (ii) long-distance migrants, originating from Europe, crossing the Mediterranean Sea and Sahara, and reaching West Africa, covering up to over 4,000 km. Despite these stark differences in migration distance, a genome-wide analysis revealed that both short- and long-distance migrants belong to a single intercontinental panmictic population extending from northern Europe to sub-Saharan Africa. Contrary to common biogeographic patterns, the Sahara is not a catalyst for population structuring in this species. No significant genetic differentiation or signs of adaptation and selection were observed between the two migratory phenotypes (pairwise FST = 0.001 {+/-} 0.006). Nonetheless, two individuals, which were early arrivals to West Africa and covered longer migration distances, exhibited some genetic differentiation. The lack of genetic structure between short- and long-distance migrants suggests that migration distance in V. cardui is a plastic response to environmental conditions. Significance statementAlthough migratory insects dominate living biomass fluxes and impact agriculture, ecosystems, and human communities, little is known about the controls of their migratory behavior. Our study develops an interdisciplinary framework, applied to the migratory butterfly V.cardui, to explore the genetic basis of variation in insect migration behavior. We leverage new generation isotope geolocation techniques to uncover striking differences in butterfly behaviour, with some individuals migrating short distances within the circum-Mediterranean region and others migrating thousands of kilometers across the Mediterranean Sea and Sahara. This major difference does not coincide with genetic differentiation or population structure and is likely a plastic response to environmental cues. This study provides a ground-breaking framework to study migration in insects.

evolutionary biology↗

Selection on many loci drove the origin and spread of a key innovation

Key innovations are fundamental to biological diversification, but their genetic architecture is poorly understood. A recent transition from egg-laying to live-bearing in Littorina snails provides the opportunity to study the architecture of an innovation that has evolved repeatedly in animals. Samples do not cluster by reproductive mode in a genome-wide phylogeny, but local genealogical analysis revealed numerous genomic regions where all live-bearers carry the same core haplotype. Associated regions show evidence for live-bearer-specific positive selection, and are enriched for genes that are differentially expressed between egg-laying and live-bearing reproductive systems. Ages of selective sweeps suggest live-bearing alleles accumulated gradually, involving selection at different times in the past. Our results suggest that innovation can have a polygenic basis, and that novel functions can evolve gradually, rather than in a single step.

evolutionary biology↗

The fine-scale recombination rate variation and associations with genomic features in a butterfly

Genetic recombination is a key molecular mechanism that has profound implications on both micro- and macro-evolutionary processes. However, the determinants of recombination rate variation in holocentric organisms are poorly understood, in particular in Lepidoptera (moths and butterflies). The wood white butterfly (Leptidea sinapis) shows considerable intraspecific variation in chromosome numbers and is a suitable system for studying regional recombination rate variation and its potential molecular underpinnings. Here, we developed a large wholegenome resequencing data set from a population of wood whites to obtain high-resolution recombination maps using linkage disequilibrium information. The analyses revealed that larger chromosomes had a bimodal recombination landscape, potentially due to interference between simultaneous chiasmata. The recombination rate was significantly lower in subtelomeric regions, with exceptions associated with segregating chromosome rearrangements, showing that fissions and fusions can have considerable effects on the recombination landscape. There was no association between the inferred recombination rate and base composition, supporting a negligible influence of GC-biased gene conversion in butterflies. We found significant but variable associations between the recombination rate and the density of different classes of transposable elements (TEs), most notably a significant enrichment of SINEs in genomic regions with higher recombination rate. Finally, the analyses unveiled significant enrichment of genes involved in farnesyltranstransferase activity in recombination cold-spots, potentially indicating that expression of transferases can inhibit formation of chiasmata during meiotic division. Our results provide novel information about recombination rate variation in holocentric organisms and has particular implications for forthcoming research in population genetics, molecular/genome evolution and speciation.

genomics↗

Migratory behavior is positively associated with genetic diversity in butterflies

Migration is typically associated with risk and uncertainty at the population level, but little is known about its cost and benefit trade-offs at the species level. Migratory insects often exhibit strong demographic fluctuations due to local bottlenecks and outbreaks. Here, we use genomic data to investigate levels of heterozygosity and long-term population size dynamics in migratory insects, as an alternative to classical local and short-term approaches such as regional field monitoring. We analyze whole-genome sequences from 97 Lepidoptera species and show that migratory species have significantly higher levels of genome-wide heterozygosity, a proxy for effective population size, than non-migratory species. Also, we contribute whole-genome data for one of the most emblematic insect migratory species, the painted lady butterfly (Vanessa cardui), sampled across its worldwide distribution range. This species exhibits one of the highest levels of heterozygosity described in Lepidoptera (2.95% {+/-} 0.15). Coalescent modeling (PSMC) shows historical demographic stability in V. cardui, and high effective population size estimates of 2 to 20 million individuals 10,000 years ago. The study reveals that the high risks associated with migration and local environmental fluctuations do not seem to decrease overall genetic diversity and demographic stability in migratory Lepidoptera. We propose a "compensatory" demographic model for migratory r-strategist organisms in which local bottlenecks are counterbalanced by reproductive success elsewhere within their typically large distributional ranges. Our findings highlight that the delimitations of populations are substantially different for sedentary and migratory insects, and that, in the latter, local and even regional field monitoring results may not reflect whole population dynamics. Genomic diversity patterns may elucidate key aspects of an insects migratory nature and population dynamics at large spatiotemporal scales.

evolutionary biology↗

Linkage mapping and genome annotation give novel insights into gene family expansions and regional recombination rate variation in the painted lady (Vanessa cardui) butterfly

Gene family expansions and crossing over are two main mechanisms for the generation of novel genetic variants that can be picked up by natural selection. Here, we developed a high-density, pedigree-based linkage map of the painted lady butterfly (Vanessa cardui) - a non-diapausing, highly polyphagous species famous for its long-distance migratory behavior. We also performed detailed annotations of genes and interspersed repetitive elements for a previously developed genome assembly, characterized species-specific gene family expansions and the relationship between recombination rate variation and genomic features. Identified expanded gene families consisted of clusters of tandem duplications with functions associated with protein and fat metabolism, detoxification, and defense against infection - key functions for the painted ladys unique lifestyle. The detailed assessment of recombination rate variation demonstrated a negative association between recombination rate and chromosome size. Moreover, the recombination landscape along the holocentric chromosomes was bimodal. The regional recombination rate was positively associated with the proportion of short interspersed elements (SINEs), but not the other repeat classes, potentially a consequence of SINEs hijacking the recombination machinery for proliferation. The detailed genetic map developed here will contribute to the understanding of the mechanisms and evolutionary consequences of recombination rate variation in Lepidoptera in general. We conclude that the structure of the painted lady genome has been shaped by a complex interplay between recombination, gene duplications and TE-activity and that specific gene family expansions have been key for the evolution of long-distance migration and the ability to utilize a wide range of host plants.

genomics↗