ABSTRACT
In their simulation study, Garcia-Costoya et al. (2023) conclude that evolutionary constraints might aid populations facing climate change. However, we are concerned that this conclusion is largely a consequence of the simulated temperature variation being too small, and, most importantly, that uneven limitations to standing variation disadvantage unconstrained populations.
Subject(s)
Biological Evolution , Climate Change , Computer Simulation , Temperature , Artifacts , Models, BiologicalABSTRACT
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.
ABSTRACT
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.
Subject(s)
Butterflies , Meiosis , Animals , Butterflies/genetics , Meiosis/genetics , Hybridization, Genetic , Karyotype , Chromosomes, Insect/genetics , Female , MaleABSTRACT
Global warming has been identified as one of the main drivers of population decline in insect pollinators. One aspect of the insect life cycle that would be particularly sensitive to elevated temperatures is the developmental transition from larva to adult. Temperature-induced modifications to the development of body parts and sensory organs likely have functional consequences for adult behaviour. To date, we have little knowledge about the effect of sub-optimal temperature on the development and functional morphology of different body parts, particularly sensory organs, in ectothermic solitary pollinators such as butterflies. To address this knowledge gap, we exposed the pupae of the butterfly Pieris napi to either 23 °C or 32 °C and measured the subsequent effects on eclosion, body size and the development of the wings, proboscis, eyes and antennae. In comparison to individuals that developed at 23 °C, we found that exposure to 32 °C during the pupal stage increased mortality and decreased time to eclose. Furthermore, both female and male butterflies that developed at 32 °C were smaller and had shorter proboscides, while males had shorter antennae. In contrast, we found no significant effect of rearing temperature on wing and eye size or wing deformity. Our findings suggest that increasing global temperatures and its corresponding co-stressors, such as humidity, will impact the survival of butterflies by impairing eclosion and the proper development of body and sensory organs.
Subject(s)
Butterflies , Humans , Male , Animals , Female , Butterflies/anatomy & histology , Temperature , Larva , Pupa , HumidityABSTRACT
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.
Subject(s)
Chromosome Aberrations , Recombination, Genetic , Humans , Polymorphism, Genetic , KaryotypeABSTRACT
Photoperiod is a common cue for seasonal plasticity and phenology, but climate change can create cue-environment mismatches for organisms that rely on it. Evolution could potentially correct these mismatches, but phenology often depends on multiple plastic decisions made during different life stages and seasons that may evolve separately. For example, Pararge aegeria (Speckled wood butterfly) has photoperiod-cued seasonal life history plasticity in two different life stages: larval development time and pupal diapause. We tested for climate change-associated evolution of this plasticity by replicating common garden experiments conducted on two Swedish populations 30 years ago. We found evidence for evolutionary change in the contemporary larval reaction norm-although these changes differed between populations-but no evidence for evolution of the pupal reaction norm. This variation in evolution across life stages demonstrates the need to consider how climate change affects the whole life cycle to understand its impacts on phenology.
Subject(s)
Butterflies , Animals , Seasons , Climate Change , Larva , Life Cycle StagesABSTRACT
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.
Subject(s)
Butterflies , Animals , Butterflies/genetics , Genome , Genomics , Genetics, Population , Recombination, GeneticABSTRACT
Climate change allows species to expand polewards, but non-changing environmental features may limit expansions. Daylength is unaffected by climate and drives life cycle timing in many animals and plants. Because daylength varies over latitudes, poleward-expanding populations must adapt to new daylength conditions. We studied local adaptation to daylength in the butterfly Lasiommata megera, which is expanding northwards along several routes in Europe. Using common garden laboratory experiments with controlled daylengths, we compared diapause induction between populations from the southern-Swedish core range and recently established marginal populations from two independent expansion fronts in Sweden. Caterpillars from the northern populations entered diapause in clearly longer daylengths than those from southern populations, with the exception of caterpillars from one geographically isolated population. The northern populations have repeatedly and rapidly adapted to their local daylengths, indicating that the common use of daylength as seasonal cue need not strongly limit climate-induced insect range expansions.
Subject(s)
Butterflies , Animals , Cues , Photoperiod , Seasons , TemperatureABSTRACT
In solitary insect pollinators such as butterflies, sensory systems must be adapted for multiple tasks, including nectar foraging, mate-finding, and locating host-plants. As a result, the energetic investments between sensory organs can vary at the intraspecific level and even among sexes. To date, little is known about how these investments are distributed between sensory systems and how it varies among individuals of different sex. We performed a comprehensive allometric study on males and females of the butterfly Pieris napi where we measured the sizes and other parameters of sensory traits including eyes, antennae, proboscis, and wings. Our findings show that among all the sensory traits measured, only antenna and wing size have an allometric relationship with body size and that the energetic investment in different sensory systems varies between males and females. Moreover, males had absolutely larger antennae and eyes, indicating that they invest more energy in these organs than females of the same body size. Overall, the findings of this study reveal that the size of sensory traits in P. napi are not necessarily related to body size and raises questions about other factors that drive sensory trait investment in this species and in other insect pollinators in general.
ABSTRACT
The evolution of host range drives diversification in phytophagous insects, and understanding the female oviposition choices is pivotal for understanding host specialization. One controversial mechanism for female host choice is Hopkins' host selection principle, where females are predicted to increase their preference for the host species they were feeding upon as larvae. A recent hypothesis posits that such larval imprinting is especially adaptive in combination with anticipatory transgenerational acclimation, so that females both allocate and adapt their offspring to their future host. We study the butterfly Pieris rapae, for which previous evidence suggests that females prefer to oviposit on host individuals of similar nitrogen content as the plant they were feeding upon as larvae, and where the offspring show higher performance on the mother's host type. We test the hypothesis that larval experience and anticipatory transgenerational effects influence female host plant acceptance (no-choice) and preference (choice) of two host plant species (Barbarea vulgaris and Berteroa incana) of varying nitrogen content. We then test the offspring performance on these hosts. We found no evidence of larval imprinting affecting female decision-making during oviposition, but that an adult female experience of egg laying in no-choice trials on the less-preferred host Be. incana slightly increased the P. rapae propensity to oviposit on Be. incana in subsequent choice trials. We found no transgenerational effects on female host acceptance or preference, but negative transgenerational effects on larval performance, because the offspring of P. rapae females that had developed on Be. incana as larvae grew slower on both hosts, and especially on Be. incana. Our results suggest that among host species, preferences are guided by hard-wired preference hierarchies linked to species-specific host traits and less affected by larval experience or transgenerational effects, which may be more important for females evaluating different host individuals of the same species.
ABSTRACT
In a time with decreasing biodiversity, especially among insects, a detailed understanding about specific resource utilization strategies is crucial. The physiological and behavioural responses to host switches in phytophagous insects are poorly understood. Earlier studies indicate that a host plant switch might be associated with distinctive molecular and physiological responses in different lineages. Expanding the assessment of such associations across Lepidoptera will reveal if there are general patterns in adaptive responses, or if each switch event is more of a unique character. We investigated host plant preference, fitness consequences, effects on expression profiles and gut microbiome composition in two common wood white (Leptidea sinapis) populations with different host plant preferences from the extremes of the species distribution area (Sweden and Catalonia). Our results show that female Catalonian wood whites lack preference for either host plant (Lotus corniculatus or L. dorycnium), while Swedish females laid significantly more eggs on L. corniculatus. Individuals from both populations reared on L. dorycnium had longer developmental times and smaller body size as adults. This indicates that both environmental and genetic factors determine the choice to use a specific host plant. Gene expression analysis revealed a more pronounced response to host plant in the Catalonian compared to the Swedish population. In addition, host plant treatment resulted in a significant shift in microbiome community structure in the Catalonian population. Together, this suggests that population specific plasticity associated with local conditions underlies host plant utilisation in wood whites.
Subject(s)
Butterflies , Microbiota , Animals , Butterflies/genetics , Diet , Female , Gene Expression , Humans , Microbiota/genetics , Sinapis , Sweden , WoodABSTRACT
Sexual dimorphism is typically thought to result from sexual selection for elaborated male traits, as proposed by Darwin. However, natural selection could reduce expression of elaborated traits in females, as proposed by Wallace. Darwin and Wallace debated the origins of dichromatism in birds and butterflies, and although evidence in birds is roughly equal, if not in favor of Wallace's model, butterflies lack a similar scale of study. Here, we present a large-scale comparative phylogenetic analysis of the evolution of butterfly coloration, using all European non-hesperiid butterfly species (n = 369). We modeled evolutionary changes in coloration for each species and sex along their phylogeny, thereby estimating the rate and direction of evolution in three-dimensional color space using a novel implementation of phylogenetic ridge regression. We show that male coloration evolved faster than female coloration, especially in strongly dichromatic clades, with male contribution to changes in dichromatism roughly twice that of females. These patterns are consistent with a classic Darwinian model of dichromatism via sexual selection on male coloration, suggesting this model was the dominant driver of dichromatism in European butterflies.
ABSTRACT
Heterozygotes for major chromosomal rearrangements such as fusions and fissions are expected to display a high level of sterility due to problems during meiosis. However, some species, especially plants and animals with holocentric chromosomes, are known to tolerate chromosomal heterozygosity even for multiple rearrangements. Here, we studied male meiotic chromosome behavior in four hybrid generations (F1-F4) between two chromosomal races of the Wood White butterfly Leptidea sinapis differentiated by at least 24 chromosomal fusions/fissions. Previous work showed that these hybrids were fertile, although their fertility was reduced as compared to crosses within chromosomal races. We demonstrate that (i) F1 hybrids are highly heterozygous with nearly all chromosomes participating in the formation of trivalents at the first meiotic division, and (ii) that from F1 to F4 the number of trivalents decreases and the number of bivalents increases. We argue that the observed process of chromosome sorting would, if continued, result in a new homozygous chromosomal race, i.e., in a new karyotype with intermediate chromosome number and, possibly, in a new incipient homoploid hybrid species. We also discuss the segregational model of karyotype evolution and the chromosomal model of homoploid hybrid speciation.
ABSTRACT
The relative role of natural selection and genetic drift in evolution is a major topic of debate in evolutionary biology. Most knowledge spring from a small group of organisms and originate from before it was possible to generate genome-wide data on genetic variation. Hence, it is necessary to extend to a larger number of taxonomic groups, descriptive and hypothesis-based research aiming at understanding the proximate and ultimate mechanisms underlying both levels of genetic polymorphism and the efficiency of natural selection. In this study, we used data from 60 whole-genome resequenced individuals of three cryptic butterfly species (Leptidea sp.), together with novel gene annotation information and population recombination data. We characterized the overall prevalence of natural selection and investigated the effects of mutation and linked selection on regional variation in nucleotide diversity. Our analyses showed that genome-wide diversity and rate of adaptive substitutions were comparatively low, whereas nonsynonymous to synonymous polymorphism and substitution levels were comparatively high in Leptidea, suggesting small long-term effective population sizes. Still, negative selection on linked sites (background selection) has resulted in reduced nucleotide diversity in regions with relatively high gene density and low recombination rate. We also found a significant effect of mutation rate variation on levels of polymorphism. Finally, there were considerable population differences in levels of genetic diversity and pervasiveness of selection against slightly deleterious alleles, in line with expectations from differences in estimated effective population sizes.
Subject(s)
Butterflies/genetics , Mutation , Selection, Genetic , Animals , Base Composition , Genetic Variation , Molecular Sequence Annotation , Recombination, GeneticABSTRACT
The male butterfly Pieris napi produces the anti-aphrodisiac pheromone methyl salicylate (MeS) and transfers it to the female during mating. After mating she releases MeS, when courted by conspecific males, which decreases her attractiveness and the duration of male harassment, thus increasing her time available for egg-laying. In previous studies we have shown that males produced MeS from the amino acid L-phenylalanine (L-Phe) acquired during larval stage. In this study we show that adult males of P. napi can utilize L-Phe and aromatic flower volatiles as building blocks for production of anti-aphrodisiac pheromone and transfer it to females during mating. We demonstrate this by feeding butterflies with stable isotope labelled molecules mixed in sugar solutions, and, to mimic the natural conditions, we fed male butterflies with floral nectar of Bunias orientalis plants treated with labelled L-Phe. The volatiles from butterflies and plants were collected and identified by solid phase micro extraction, gas chromatography and mass spectrometry techniques. Since P. napi is polygamous, males would gain from restoring the titre of MeS after mating and the use of aromatic precursors for production of MeS could be considered as an advantageous trait which could enable butterflies to relocate L-Phe for other needs.
Subject(s)
Aphrodisiacs/antagonists & inhibitors , Butterflies/physiology , Pheromones/metabolism , Salicylates/metabolism , Sexual Behavior, Animal , Animals , Female , Male , Phenylalanine/metabolismABSTRACT
Genome scans in recently separated species can inform on molecular mechanisms and evolutionary processes driving divergence. Large-scale polymorphism data from multiple species pairs are also key to investigate the repeatability of divergence-whether radiations tend to show parallel responses to similar selection pressures and/or underlying molecular forces. Here, we used whole-genome resequencing data from six wood white (Leptidea sp.) butterfly populations, representing three closely related species with karyomorph variation, to infer the species' demographic history and characterize patterns of genomic diversity and differentiation. The analyses supported previously established species relationships, and there was no evidence for postdivergence gene flow. We identified significant intraspecific genetic structure, in particular between karyomorph extremes in the wood white (L. sinapis)-a species with a remarkable chromosome number cline across the distribution range. The genomic landscapes of differentiation were erratic, and outlier regions were narrow and dispersed. Highly differentiated (FST ) regions generally had low genetic diversity (θπ ), but increased absolute divergence (DXY ) and excess of rare frequency variants (low Tajima's D). A minority of differentiation peaks were shared across species and population comparisons. However, highly differentiated regions contained genes with overrepresented functions related to metabolism, response to stimulus and cellular processes, indicating recurrent directional selection on a specific set of traits in all comparisons. In contrast to the majority of genome scans in recently diverged lineages, our data suggest that divergence landscapes in Leptidea have been shaped by directional selection and genetic drift rather than stable recombination landscapes and/or introgression.
Subject(s)
Butterflies/genetics , Gene Flow , Genetic Speciation , Genetics, Population , Animals , Asia , Bacterial Proteins , Butterflies/classification , DNA, Mitochondrial/genetics , Europe , Gene Frequency , Genetic Variation , Genome , Repressor Proteins , Selection, Genetic , Whole Genome SequencingABSTRACT
Chromosome evolution presents an enigma in the mega-diverse Lepidoptera. Most species exhibit constrained chromosome evolution with nearly identical haploid chromosome counts and chromosome-level gene collinearity among species more than 140 million years divergent. However, a few species possess radically inflated chromosomal counts due to extensive fission and fusion events. To address this enigma of constraint in the face of an exceptional ability to change, we investigated an unprecedented reorganization of the standard lepidopteran chromosome structure in the green-veined white butterfly (Pieris napi). We find that gene content in P. napi has been extensively rearranged in large collinear blocks, which until now have been masked by a haploid chromosome number close to the lepidopteran average. We observe that ancient chromosome ends have been maintained and collinear blocks are enriched for functionally related genes suggesting both a mechanism and a possible role for selection in determining the boundaries of these genome-wide rearrangements.
Subject(s)
Butterflies/genetics , Chromosomes, Insect/chemistry , Evolution, Molecular , Genome, Insect , Animals , Bombyx/classification , Bombyx/genetics , Butterflies/classification , Chromosome Mapping , Female , Genetic Linkage , Genome Size , Male , Phylogeny , Ploidies , Selection, GeneticABSTRACT
A method for analysis of proteins from spermatophores transferred from male to female Pieris napi butterflies during mating has been developed. The proteins were solubilized from the dissected spermatophores using different solubilization agents (water, methanol, acetonitrile and hexafluoroisopropanol). Capillary electrophoresis (CE) analysis was performed using an acidic background electrolyte containing a fluorosurfactant to avoid protein-wall adsorption, and to increase separation performance. The samples were also analyzed with matrix assisted laser desorption/ionization mass spectrometry (MALDI-MS), in a lower m/z range (1000-6000) and a higher m/z range (6000-12000). Solubilization with different solvents and the use of alternative matrices gave partly complementary profiles.
Subject(s)
Butterflies/chemistry , Electrophoresis, Capillary/methods , Insect Proteins/analysis , Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization/methods , Spermatogonia/chemistry , Animals , Male , Solvents/chemistryABSTRACT
Chromosomal rearrangements (e.g., fusions/fissions) have the potential to drive speciation. However, their accumulation in a population is generally viewed as unlikely, because chromosomal heterozygosity should lead to meiotic problems and aneuploid gametes. Canonical meiosis involves segregation of homologous chromosomes in meiosis I and sister chromatid segregation during meiosis II. In organisms with holocentric chromosomes, which are characterized by kinetic activity distributed along almost the entire chromosome length, this order may be inverted depending on their metaphase I orientation. Here we analyzed the evolutionary role of this intrinsic versatility of holocentric chromosomes, which is not available to monocentric ones, by studying F1 to F4 hybrids between two chromosomal races of the Wood White butterfly (Leptidea sinapis), separated by at least 24 chromosomal fusions/fissions. We found that these chromosomal rearrangements resulted in multiple meiotic multivalents, and, contrary to the theoretical prediction, the hybrids displayed relatively high reproductive fitness (42% of that of the control lines) and regular behavior of meiotic chromosomes. In the hybrids, we also discovered inverted meiosis, in which the first and critical stage of chromosome number reduction was replaced by the less risky stage of sister chromatid separation. We hypothesize that the ability to invert the order of the main meiotic events facilitates proper chromosome segregation and hence rescues fertility and viability in chromosomal hybrids, potentially promoting dynamic karyotype evolution and chromosomal speciation.
Subject(s)
Butterflies , Chimera , Chromatids , Metaphase/physiology , Animals , Butterflies/genetics , Butterflies/metabolism , Chimera/genetics , Chimera/metabolism , Chromatids/genetics , Chromatids/metabolism , Chromosomes, Insect/genetics , Chromosomes, Insect/metabolismABSTRACT
In temperate latitudes, many insects enter diapause (dormancy) during the cold season, a period during which developmental processes come to a standstill. The wood white (Leptidea sinapis) is a butterfly species distributed across western Eurasia that shows photoperiod-induced diapause with variation in critical day-length across populations at different latitudes. We assembled transcriptomes and estimated gene expression levels at different developmental stages in experimentally induced directly developing and diapausing cohorts of a single Swedish population of L. sinapis to investigate the regulatory mechanisms underpinning diapause initiation. Different day lengths resulted in expression changes of developmental genes and affected the rate of accumulation of signal molecules, suggesting that diapause induction might be controlled by increased activity of monoamine neurotransmitters in larvae reared under short-day light conditions. Expression differences between light treatment groups of two monoamine regulator genes (DDC and ST) were observed already in instar III larvae. Once developmental pathways were irreversibly set at instar V, a handful of genes related to dopamine production were differentially expressed leading to a significant decrease in expression of global metabolic genes and increase in expression of genes related to fatty acid synthesis and sequestration. This is in line with a time-dependent (hour-glass) model of diapause regulation where a gradual shift in the concentration of monoamine neurotransmitters and their metabolites during development of larvae under short-day conditions leads to increased storage of fat, decreased energy expenditures, and ultimately developmental stasis at the pupal stage.