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Talavera, G.

Publications and source records attributed to Talavera, G..

11 recordsLinked to original sources

Size- and colour-based mechanisms shape the phenological structure of butterfly communities

O_LISeasonal patterns of species appearances constitute a major component of diversity variation. Theory attributes this phenological structuring of communities to the alignment of life cycles to suitable moments and to constraints of seasonality on development, yet the specific mechanisms operating across taxa remain largely unresolved. In insects, body size and colour are key functional traits that contribute to driving spatial community assembly through their link to thermoregulatory performance and development. C_LIO_LIHere we analyse variation in mean body size and colour lightness of 483 butterfly assemblages across Great Britain and throughout the season to test whether trait alignment with seasonal environment and developmental constraints may shape the phenological structuring of communities. C_LIO_LIBoth body size and body colour varied more along season than across space, emphasizing the importance of phenology on diversity variation. Body size was larger early and late in the season, i.e. under conditions of low temperature and solar radiation. This pattern contrasted with the spatial trends found and was driven by species overwintering as adults, which we interpret as being likely due to energetic constraints. Body colour, conversely, was darker early and late in the season, mirroring the spatial pattern found, and suggesting a thermoregulatory alignment with seasonal conditions. Furthermore, covariation between body size and colour suggests a thermoregulatory interaction between both traits. C_LIO_LIOur findings suggest that life-cycle constraints and seasonal thermoregulatory alignment contribute to shaping the phenological structure of insect communities. C_LI

ecology↗

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↗

Polyommatine blue butterflies reveal unexpected integrity of the W sex chromosome amid extensive chromosome fragmentation

Chromosomal rearrangements are crucial in speciation, acting as barriers to gene flow. Holocentric chromosomes, such as those in Lepidoptera, can facilitate karyotype changes. Despite chromosome fusions being more common, speciation events are mostly linked to fissions. Notable karyotypic variation is observed in three clades of the subfamily Polyommatinae (Lycaenidae), with chromosome numbers ranging from n = 10 to n = 225. This study used flow cytometry and molecular cytogenetic analyses to investigate genome sizes and karyotypes in several species of the genera Polyommatus and Lysandra with derived and modal chromosome numbers. The findings show no support for polyploidy, supporting karyotypic diversification via fragmentation of chromosomes. Species with high chromosome numbers have larger genomes, which indicates a potential role of mobile elements but contradicts the hypothesis of holocentric drive. Telomeric signals were detected at the ends of fragmented chromosomes. No interstitial telomeric sequences were detected on autosomes. Interstitial telomeric signals on sex chromosomes, however, revealed multiple sex chromosome systems in Polyommatus dorylas and Polyommatus icarus, with two karyotype races differing in sex chromosome constitution in the latter. Pool-seq and coverage analyses indicated shared fusion of sex chromosomes with an autosome bearing the rDNA locus, followed by a fusion with chromosome 20 in the Czech population. Notably, the W chromosome resists fragmentation, likely due to epigenetic silencing protecting it from activity of mobile elements.

genomics↗

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↗

Transposable element insertions are associated with Batesian mimicry in the pantropical butterfly Hypolimnas misippus

Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate the four colour morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved a wing pattern present in other Hypolimnas species for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, we discover two large transposable element (TE) insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing the ancestral and mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that the TEs disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.

evolutionary biology↗

Environmental stress during larval development induces head methylome profile shifts in the migratory painted lady butterfly (Vanessa cardui)

Seasonal environmental fluctuations provide formidable challenges for living organisms, especially small ectotherms such as butterflies. A common strategy to cope with harsh environments is to enter diapause, but some species avoid the unsuitable conditions by migrating. Despite a growing understanding of migration in the life cycles of some butterfly species, it is unknown how individuals register and store environmental cues to determine whether and where to migrate. Here, we explored how competition and host plant availability during larval development affect patterns of DNA methylation in the migratory painted lady (Vanessa cardui) butterfly. We identify a set of potentially functional methylome shifts associated with differences in the environment, indicating that DNA methylation is involved in the response to different conditions during larval development. By analysing the transcriptome for the same samples used for methylation profiling, we also uncovered a non-linear relationship between gene body methylation and gene expression. Our results provide a starting point for understanding the interplay between DNA methylation and gene expression in butterflies in general and how differences in environmental conditions during development can trigger unique epigenetic marks that might be important for behavioural decisions in the adult stage.

evolutionary biology↗

Metals and metal isotopes in insect wings: Implications for diet, geolocation and pollution exposure

Anthropogenic activities are exposing insects to abnormal levels of toxic metals, with unknown implications for migratory insects. Simultaneously, metals and metal isotopes have become promising tools for the geolocation of migratory insects. Furthering our understanding of metal cycling in insect tissues is essential, both for the development of metals and metal isotopes as geolocation tools, and for assessing the toxicity risks of metals to insects. We conducted a diet-switching experiment on monarch butterflies (Danaus plexippus) with controlled larval and adult diets to evaluate the dietary and environmental sources of 23 metals and metalloids, strontium isotopes, and lead isotopes to insect wing tissues over a period of 8 weeks. Concentrations of Ca, Co, and Sb differed between the sexes. Ni and Zn bioaccumulated in the insect wing tissues over time, likely from the adult diet, while increases in Al, Cr, Cd, Cu, Fe, and Pb were likely from external sources (i.e., dust aerosols). Bioaccumulation of Pb in the monarch wings was confirmed by Pb isotopes to be from external anthropogenic sources, revealing the potential of Pb isotopes to become an indicator and tracer of metal pollution exposure along migratory paths. Concentrations of Ba, Cs, Mg, Na, Rb, Sr, Ti, Tl, and U appeared to be unaffected by dietary or environmental contamination and should be further developed for geolocation purposes. Strontium isotope ratios remained indicative of the larval diet, at least in males, supporting its potential as a geolocation tool. However, the difference in strontium isotope ratios between sexes, as well as the possibility of external contamination by wetting, requires further investigation. Our results demonstrate the complexity of metal cycling in insects and the need for further investigations, as well as the value of studying metals to develop new tools to quantify pollution exposure, metal toxicity and insect mobility.

ecology↗

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↗

Global invasion history of the world’s most abundant pest butterfly: a citizen science population genomics study

A major goal of invasion and climate change biology research is to understand the ecological and evolutionary responses of organisms to anthropogenic disturbance, especially over large spatial and temporal scales. One significant, and sometimes unattainable, challenge of these studies is garnering sufficient numbers of relevant specimens, especially for species spread across multiple continents. We developed a citizen science project, \"Pieris Project\", to successfully amass thousands of specimens of the invasive agricultural pest Pieris rapae, the small cabbage white butterfly, from 32 countries worldwide. We then generated and analyzed genomic (ddRAD) and mitochondrial DNA sequence data for these samples to reconstruct and compare different global invasion history scenarios. Our results bolster historical accounts of the global spread and timing of P. rapae introductions. The spread of P. rapae over the last [~]160 years followed a linear series of at least four founding events, with each introduced population serving as the source for the next. We provide the first molecular evidence supporting the hypothesis that the ongoing divergence of the European and Asian subspecies of P. rapae ([~]1,200 yrBP) coincides with the domestication of brassicaceous crops. Finally, the international success of the Pieris Project allowed us to nearly double the geographic scope of our sampling (i.e., add >1,000 specimens from 13 countries), demonstrating the power of the public to aid scientists in collections-based research addressing important questions in ecology and evolutionary biology.\n\nNon-technical summaryWe provide genetic evidence that the success of the small cabbage white butterfly--its rise to one of the most widespread and abundant butterflies on the planet-- was largely facilitated by human activities, through the domestication of its food plants and the accidental movement of the butterfly by means of trade and human movement (migration). Through an international citizen science project--Pieris Project--people from around the world helped to unravel the global invasion history of this agricultural pest butterfly by collecting samples for DNA analysis. The success of this citizen science project demonstrates the power of the public to aid in collections-based research that address important questions related to ecology and evolutionary biology.

evolutionary biology↗

Pollen metabarcoding as a tool for tracking long-distance insect migrations.

Insects account for the main fraction of Earths biodiversity and are key players for ecosystems, notably as pollinators. While insect migration is suspected to represent a natural phenomenon of major importance, remarkably little is known about it, except for a few flagship species. The reason for this situation is mainly due to technical limitations in the study of insect movement. Here we propose using metabarcoding of pollen carried by insects as a method for tracking their migrations. We developed a flexible and simple protocol allowing high multiplexing and not requiring DNA extraction, one of the most time consuming part of metabarcoding protocols, and apply this method to the study of the longdistance migration of the butterfly Vanessa cardui, an emerging model for insect migration. We collected 47 butterfly samples along the Mediterranean coast of Spain in spring and performed metabarcoding of pollen collected from their bodies to test for potential arrivals from the African continent. In total, we detected 157 plant species from 23 orders, most of which (82.8%) were insect-pollinated. African or African-Arabian endemic taxa contributed 21.0% of our dataset, strongly supporting the hypothesis that migratory butterflies colonize southern Europe from Africa in spring. Moreover, our data suggest that a northwards trans-Saharan migration in spring is plausible for early arrivals (February) into Europe, as shown by the presence of Saharan floristic elements. Our results demonstrate the possibility of regular insect-mediated transcontinental pollination, with potential implications for ecosystem functioning, agriculture and plant phylogeography. Despite current limitations, mostly regarding the availability of plant reference sequences and distribution data, the method proved to be useful and demonstrates great potential as plant genetic libraries and distribution datasets improve.

ecology↗