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Natural selection is less efficient in the absence of recombination. As a result, nonrecombining sequences, such as sex chromosomes, tend to degenerate over time. Although the outcomes of recombination arrest are typically observed after many millions of generations, recent neo-sex chromosomes can give insight into the early stages of this process. Here, we investigate the evolution of neo-sex chromosomes in the Spanish marbled white butterfly, Melanargia ines, where a Z-autosome fusion has turned the homologous autosome into a nonrecombining neo-W chromosome. We show that these neo-sex chromosomes are likely limited to the Iberian population of M. ines, and that they arose around the time when this population split from North-African populations, around 1.5 million years ago. Recombination arrest of the neo-W chromosome has led to an excess of premature stop-codons and frame-shift mutations, and reduced gene expression compared to the neo-Z chromosome. Surprisingly, we identified two regions of â¼1 Mb at one end of the neo-W that are both less diverged from the neo-Z and less degraded than the rest of the chromosome, suggesting a history of rare but repeated genetic exchange between the two neo-sex chromosomes. These plateaus of neo-sex chromosome divergence suggest that neo-W degradation can be locally reversed by rare recombination between neo-W and neo-Z chromosomes.
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Mariposas Diurnas , Recombinación Genética , Cromosomas Sexuales , Animales , Cromosomas Sexuales/genética , Masculino , Mariposas Diurnas/genética , Femenino , Evolución Molecular , Selección GenéticaRESUMEN
Migratory insects may move in large numbers, even surpassing migratory vertebrates in biomass. Long-distance migratory insects complete annual cycles through multiple generations, with each generation's reproductive success linked to the resources available at different breeding grounds. Climatic anomalies in these grounds are presumed to trigger rapid population outbreaks. Here, we infer the origin and track the multigenerational path of a remarkable outbreak of painted lady (Vanessa cardui) butterflies that took place at an intercontinental scale in Europe, the Middle East, and Africa from March 2019 to November 2019. Using metabarcoding, we identified pollen transported by 264 butterflies captured in 10 countries over 7 months and modeled the distribution of the 398 plants detected. The analysis showed that swarms collected in Eastern Europe in early spring originated in Arabia and the Middle East, coinciding with a positive anomaly in vegetation growth in the region from November 2018 to April 2019. From there, the swarms advanced to Northern Europe during late spring, followed by an early reversal toward southwestern Europe in summer. The pollen-based evidence matched spatiotemporal abundance peaks revealed by citizen science, which also suggested an echo effect of the outbreak in West Africa during September-November. Our results show that population outbreaks in a part of species' migratory ranges may disseminate demographic effects across multiple generations in a wide geographic area. This study represents an unprecedented effort to track a continuous multigenerational insect migration on an intercontinental scale.
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Migración Animal , Mariposas Diurnas , Código de Barras del ADN Taxonómico , Polen , Animales , Mariposas Diurnas/fisiología , Europa (Continente)/epidemiología , Medio Oriente/epidemiología , África/epidemiología , Estaciones del AñoRESUMEN
The extent of aerial flows of insects circulating around the planet and their impact on ecosystems and biogeography remain enigmatic because of methodological challenges. Here we report a transatlantic crossing by Vanessa cardui butterflies spanning at least 4200 km, from West Africa to South America (French Guiana) and lasting between 5 and 8 days. Even more, we infer a likely natal origin for these individuals in Western Europe, and the journey Europe-Africa-South America could expand to 7000 km or more. This discovery was possible through an integrative approach, including coastal field surveys, wind trajectory modelling, genomics, pollen metabarcoding, ecological niche modelling, and multi-isotope geolocation of natal origins. The overall journey, which was energetically feasible only if assisted by winds, is among the longest documented for individual insects, and potentially the first verified transatlantic crossing. Our findings suggest that we may be underestimating transoceanic dispersal in insects and highlight the importance of aerial highways connecting continents by trade winds.
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Mariposas Diurnas , Vuelo Animal , Animales , Mariposas Diurnas/fisiología , Vuelo Animal/fisiología , Viento , Ecosistema , América del Sur , Europa (Continente) , Migración Animal/fisiología , Polen , África , Distribución AnimalRESUMEN
Species frequently differ in the number and structure of chromosomes they harbor, but individuals that are heterozygous for chromosomal rearrangements may suffer from reduced fitness. Chromosomal rearrangements like fissions and fusions can hence serve as a mechanism for speciation between incipient lineages, but their evolution poses a paradox. How can rearrangements get fixed between populations if heterozygotes have reduced fitness? One solution is that this process predominantly occurs in small and isolated populations, where genetic drift can override natural selection. However, fixation is also more likely if a novel rearrangement is favored by a transmission bias, such as meiotic drive. Here, we investigate chromosomal transmission distortion in hybrids between two wood white (Leptidea sinapis) butterfly populations with extensive karyotype differences. Using data from two different crossing experiments, we uncover that there is a transmission bias favoring the ancestral chromosomal state for derived fusions, a result that shows that chromosome fusions actually can fix in populations despite being counteracted by meiotic drive. This means that meiotic drive not only can promote runaway chromosome number evolution and speciation, but also that it can be a conservative force acting against karyotypic change and the evolution of reproductive isolation. Based on our results, we suggest a mechanistic model for why chromosome fusion mutations may be opposed by meiotic drive and discuss factors contributing to karyotype evolution in Lepidoptera.
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Mariposas Diurnas , Meiosis , Animales , Mariposas Diurnas/genética , Meiosis/genética , Hibridación Genética , Cariotipo , Cromosomas de Insectos/genética , Femenino , MasculinoRESUMEN
The number of known alien ant species throughout Europe has been steadily increasing during the last few decades and Italy has been no exception, with four new taxa reported in the last five years. Here, we document new data on the Asian needle ant Brachyponerachinensis (Emery, 1895), an invasive alien species whose first establishment in Europe was detected in the southern Italian city of Naples in 2022 and which has now been found near Lake Como in northern Italy, representing the second European record, about 730 km distant from the first. Furthermore, we report for the first time the presence of Nylanderiavividula (Nylander, 1846) in the country, based on specimens collected both in Rome and near Lake Como. This is at least the second Nylanderia species established in the country after N.jaegerskioeldi, first reported in 2018. Unlike B.chinensis, N.vividula is not considered an ecological and health threat in the invaded range and is already known to occur in several other European countries. While only a few introduced ants in Europe are considered serious ecological, economic or health threats, the increasing circulation of several alien species and the poor ability to swiftly track their movements and detect their establishment can render management very difficult.
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The faster-Z/X hypothesis predicts that sex-linked genes should diverge faster than autosomal genes. However, studies across different lineages have shown mixed support for this effect. So far, most analyses have focused on old and well differentiated sex chromosomes, but less is known about divergence of more recently acquired neo-sex chromosomes. In Lepidoptera (moths and butterflies), Z-autosome fusions are frequent, but the evolutionary dynamics of neo-Z chromosomes have not been explored in detail. Here, we analysed the faster-Z effect in Leptidea sinapis, a butterfly with three Z chromosomes. We show that the neo-Z chromosomes have been acquired stepwise, resulting in strata of differentiation and masculinization. While all Z chromosomes showed evidence of the faster-Z effect, selection for genes on the youngest neo-Z chromosome (Z3) appears to have been hampered by a largely intact, homologous neo-W chromosome. However, the intermediately aged neo-Z chromosome (Z2), which lacks W gametologs, showed less evolutionary constraints, resulting in particularly fast evolution. Our results therefore support that neo-sex chromosomes can constitute temporary hot-spots of adaptation and divergence. The underlying dynamics are likely causally linked to shifts in selective constraints, evolution of gene expression, and degeneration of W-linked gametologs which gradually expose Z-linked genes to selection.
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The impact of large-scale chromosomal rearrangements, such as fusions and fissions, on speciation is a long-standing conundrum. We assessed whether bursts of change in chromosome numbers resulting from chromosomal fusion or fission are related to increased speciation rates in Erebia, one of the most species-rich and karyotypically variable butterfly groups. We established a genome-based phylogeny and used state-dependent birth-death models to infer trajectories of karyotype evolution. We demonstrated that rates of anagenetic chromosomal changes (i.e., along phylogenetic branches) exceed cladogenetic changes (i.e., at speciation events), but, when cladogenetic changes occur, they are mostly associated with chromosomal fissions rather than fusions. We found that the relative importance of fusion and fission differs among Erebia clades of different ages and that especially in younger, more karyotypically diverse clades, speciation is more frequently associated with cladogenetic chromosomal changes. Overall, our results imply that chromosomal fusions and fissions have contrasting macroevolutionary roles and that large-scale chromosomal rearrangements are associated with bursts of species diversification.
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Mariposas Diurnas , Animales , Filogenia , Mariposas Diurnas/genética , Cariotipo , Cariotipificación , Aberraciones Cromosómicas , Evolución MolecularRESUMEN
Temperature is thought to be a key factor influencing global species richness patterns. We investigate the link between temperature and diversification in the butterfly family Pieridae by combining next generation DNA sequences and published molecular data with fine-grained distribution data. We sampled nearly 600 pierid butterfly species to infer the most comprehensive molecular phylogeny of the family and curated a distribution dataset of more than 800,000 occurrences. We found strong evidence that species in environments with more stable daily temperatures or cooler maximum temperatures in the warm seasons have higher speciation rates. Furthermore, speciation and extinction rates decreased in tandem with global temperatures through geological time, resulting in a constant net diversification.
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Glacial cycles lead to periodic population interbreeding and isolation in warm-adapted species, which impact genetic structure and evolution. However, the effects of these processes on highly mobile and more cold-tolerant species are not well understood. This study aims to shed light on the phylogeographic history of Aglais urticae, a butterfly species with considerable dispersal ability, and a wide Palearctic distribution reaching the Arctic. Through the analysis of genomic data, four main genetic lineages are identified: European, Sierra Nevada, Sicily/Calabria/Peloponnese, and Eastern. The results indicate that the Sardo-Corsican endemic taxon ichnusa is a distinct species. The split between the relict lineages in southern Europe and the main European lineage is estimated to have happened 400-450 thousand years ago, with admixture observed during the Quaternary glacial cycles, and still ongoing, albeit to a much smaller extent. These results suggest that these lineages may be better treated as subspecific parapatric taxa. Ecological niche modelling supported the existence of both Mediterranean and extra-Mediterranean refugia during the glacial periods, with the main one located on the Atlantic coast. Nevertheless, gene flow between populations was possible, indicating that both differentiation and admixture have acted continuously across glacial cycles in this cold-tolerant butterfly, generally balancing each other but producing differentiated lineages in the southern peninsulas. We conclude that the population dynamics and the processes shaping the population genetic structure of cold-adapted species during the Quaternary ice ages may be different than those classically accepted for warm-adapted species.
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Mariposas Diurnas , Variación Genética , Animales , Filogenia , Variación Genética/genética , Mariposas Diurnas/genética , Filogeografía , Europa (Continente)RESUMEN
Menchetti et al. respond to the letter of Genovesi et al. and contribute new records of the red imported fire ant in Sicily.
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Hormigas , Biovigilancia , Animales , SiciliaRESUMEN
RATIONALE: Many insect species undertake multigenerational migrations in the Afro-tropical and Palearctic ranges, and understanding their migratory connectivity remains challenging due to their small size, short life span and large population sizes. Hydrogen isotopes (δ2 H) can be used to reconstruct the movement of dispersing or migrating insects, but applying δ2 H for provenance requires a robust isotope baseline map (i.e. isoscape) for the Afro-Palearctic. METHODS: We analyzed the δ2 H in the wings (δ2 Hwing ) of 142 resident butterflies from 56 sites across the Afro-Palearctic. The δ2 Hwing values were compared to the predicted local growing-season precipitation δ2 H values (δ2 HGSP ) using a linear regression model to develop an insect wing δ2 H isoscape. We used multivariate linear mixed models and high-resolution and time-specific remote sensing climate and environmental data to explore the controls of the residual δ2 Hwing variability. RESULTS: A strong linear relationship was found between δ2 Hwing and δ2 HGSP values (r2 = 0.53). The resulting isoscape showed strong patterns across the Palearctic but limited variation and high uncertainty for the Afro-tropics. Positive residuals of this relationship were correlated with dry conditions for the month preceding sampling whereas negative residuals were correlated with more wet days for the month preceding sampling. High intra-site δ2 Hwing variance was associated with lower relative humidity for the month preceding sampling and higher elevation. CONCLUSION: The δ2 Hwing isoscape is applicable for tracing herbivorous lepidopteran insects that migrate across the Afro-Palearctic range but has limited geolocation potential in the Afro-tropics. The spatial analysis of uncertainty using high-resolution climatic data demonstrated that many African regions with highly variable evaporation rates and relative humidity have δ2 Hwing values that are less related to δ2 HGSP values. Increasing geolocation precision will require new modeling approaches using more time-specific environmental data and/or independent geolocation tools.
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Mariposas Diurnas , Animales , Hidrógeno , Isótopos/análisis , Estaciones del Año , Modelos LinealesRESUMEN
Large-scale chromosome rearrangements, such as fissions and fusions, are a common feature of eukaryote evolution. They can have considerable influence on the evolution of populations, yet it remains unclear exactly how rearrangements become established and eventually fix. Rearrangements could fix by genetic drift if they are weakly deleterious or neutral, or they may instead be favoured by positive natural selection. Here, we compare genome assemblies of three closely related Brenthis butterfly species and characterize a complex history of fission and fusion rearrangements. An inferred demographic history of these species suggests that rearrangements became fixed in populations with large long-term effective size (Ne ), consistent with rearrangements being selectively neutral or only very weakly underdominant. Using a recently developed analytic framework for characterizing hard selective sweeps, we find that chromosome fusions are not enriched for evidence of past sweeps compared to other regions of the genome. Nonetheless, we do infer a strong and recent selective sweep around one chromosome fusion in the B. daphne genome. Our results suggest that rearrangements in these species likely have weak absolute fitness effects and fix by genetic drift. However, one putative selective sweep raises the possibility that natural selection may sometimes play a role in the fixation of chromosome fusions.
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The red imported fire ant (Solenopsis invicta) is classified as one of the worst invasive alien species1 and as the fifth costliest worldwide2, impacting ecosystems, agriculture and human health3. We report the establishment of S. invicta in Europe for the first time, documenting a mature population in Sicily. We use genetic analyses to assess its putative origin, as well as wind tracking and species distribution modelling to predict its potential range on the continent. We show that half of the urban areas in Europe are already suitable and that climate warming expected under current trends will favor the expansion of this invasive ant.
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Hormigas , Humanos , Animales , Hormigas/genética , Ecosistema , Europa (Continente) , Agricultura , Clima , Especies IntroducidasRESUMEN
We present a genome assembly from an individual female Ochlodes sylvanus, the Large Skipper (Arthropoda; Insecta; Lepidoptera; Hesperiidae). The genome sequence is 380 megabases in span. Most of the assembly (99.97%) is scaffolded into 30 chromosomal pseudomolecules, including the assembled W and Z sex chromosomes. The mitochondrial genome has also been assembled and is 17.1 kilobases in length. Gene annotation of this assembly on Ensembl identified 13,451 protein coding genes.
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Reshuffling of genetic variation occurs both by independent assortment of chromosomes and by homologous recombination. Such reshuffling can generate novel allele combinations and break linkage between advantageous and deleterious variants which increases both the potential and the efficacy of natural selection. Here we used high-density linkage maps to characterize global and regional recombination rate variation in two populations of the wood white butterfly (Leptidea sinapis) that differ considerably in their karyotype as a consequence of at least 27 chromosome fissions and fusions. The recombination data were compared to estimates of genetic diversity and measures of selection to assess the relationship between chromosomal rearrangements, crossing over, maintenance of genetic diversity and adaptation. Our data show that the recombination rate is influenced by both chromosome size and number, but that the difference in the number of crossovers between karyotypes is reduced as a consequence of a higher frequency of double crossovers in larger chromosomes. As expected from effects of selection on linked sites, we observed an overall positive association between recombination rate and genetic diversity in both populations. Our results also revealed a significant effect of chromosomal rearrangements on the rate of intergenic diversity change between populations, but limited effects on polymorphisms in coding sequence. We conclude that chromosomal rearrangements can have considerable effects on the recombination landscape and consequently influence both maintenance of genetic diversity and efficiency of selection in natural populations.
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Aberraciones Cromosómicas , Recombinación Genética , Humanos , Polimorfismo Genético , CariotipoRESUMEN
A new subspecies of Leptideasinapis from Northern Iran, discovered by means of DNA barcoding, is described as Leptideasinapistabarestanassp. nov. The new subspecies is allopatric with respect to other populations of L.sinapis and is genetically distinct, appearing as a well-supported sister clade to all other populations in COI-based phylogenetic reconstructions. Details on karyotype, genitalia, ecology and behaviour for the new subspecies are given and a biogeographical speciation scenario is proposed.
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Recombination is a key molecular mechanism that has profound implications on both micro- and macroevolutionary 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 whole-genome 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 caused by 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 limited 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, most notably a significant enrichment of short interspersed nucleotide elements in genomic regions with higher recombination rate. Finally, the analyses unveiled significant enrichment of genes involved in farnesyltranstransferase activity in recombination coldspots, 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 have particular implications for forthcoming research in population genetics, molecular/genome evolution, and speciation.
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Mariposas Diurnas , Animales , Mariposas Diurnas/genética , Genoma , Genómica , Genética de Población , Recombinación GenéticaRESUMEN
There are only two Aphaenogaster species from the subterranea group in the western Mediterranean: A.ichnusa Santschi, 1925, from south-western Europe, and A.subterranea (Latreille, 1798), also occurring in central and eastern Europe. Historically, the two species have been widely misunderstood: A.ichnusa was long considered a Sardinian endemic subspecies of A.subterranea, while its continental populations were misidentified as A.subterranea s. str. Recently, A.ichnusa was elevated to species rank and its worker caste was redescribed with that of A.subterranea, allowing for their correct identification. Yet their distribution was documented in detail only for France and Sardinia. Furthermore, no morphological characters were described to distinguish the males and queens of the two species. By investigating private and museum collections, 276 new records of A.ichnusa are provided here and 154 of A.subterranea from the western Mediterranean. Additionally, qualitative and quantitative morphological characters were combined to identify their males and queens. We present the new southernmost, easternmost, and westernmost distribution limits for A.ichnusa. Based on our results, this species is widely distributed in Italy and Catalonia (Spain), also occurring on several Mediterranean islands, avoiding areas with continental climate and high altitudes. Sicily is the only island to host the less thermophilous A.subterranea, which otherwise extends westward to Galicia (Spain). Sympatric occurrence is not rare along the contact zone. Additional natural history observations are reported regarding foraging habits, associated myrmecophiles, habitat preferences, and colony structure in the two species.
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Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto-predaceous Lepidochrysops butterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time-calibrated phylogeny for Lepidochrysops and its closest, non-parasitic relatives in the Euchrysops section (Poloyommatini). We estimated ancestral areas across the phylogeny with process-based biogeographical models and diversification rates relying on time-variable and clade-heterogeneous birth-death models. The Euchrysops section originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto-predaceous Lepidochrysops lineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of the Euchrysops section, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto-predaceous life history in species of Lepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.
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Migratory insects are key players in ecosystem functioning and services, but their spatiotemporal distributions are typically poorly known. Ecological niche modeling (ENM) may be used to predict species seasonal distributions, but the resulting hypotheses should eventually be validated by field data. The painted lady butterfly (Vanessa cardui) performs multigenerational migrations between Europe and Africa and has become a model species for insect movement ecology. While the annual migration cycle of this species is well understood for Europe and northernmost Africa, it is still unknown where most individuals spend the winter. Through ENM, we previously predicted suitable breeding grounds in the subhumid regions near the tropics between November and February. In this work, we assess the suitability of these predictions through i) extensive field surveys and ii) two-year monitoring in six countries: a large-scale monitoring scheme to study butterfly migration in Africa. We document new breeding locations, year-round phenological information, and hostplant use. Field observations were nearly always predicted with high probability by the previous ENM, and monitoring demonstrated the influence of the precipitation seasonality regime on migratory phenology. Using the updated dataset, we built a refined ENM for the Palearctic-African range of V. cardui. We confirm the relevance of the Afrotropical region and document the missing natural history pieces of the longest migratory cycle described in butterflies.