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- Carnicer, Jofre, et al.
(author)
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Phenotypic biomarkers of climatic impacts on declining insect populations : A key role for decadal drought, thermal buffering and amplification effects and host plant dynamics
- 2019
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In: Journal of Animal Ecology. - : Wiley. - 0021-8790 .- 1365-2656. ; 88:3, s. 376-391
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Journal article (peer-reviewed)abstract
- Widespread population declines have been reported for diverse Mediterranean butterflies over the last three decades, and have been significantly associated with increased global change impacts. The specific landscape and climatic drivers of these declines remain uncertain for most declining species. Here, we analyse whether plastic phenotypic traits of a model butterfly species (Pieris napi) perform as reliable biomarkers of vulnerability to extreme temperature impacts in natural populations, showing contrasting trends in thermally exposed and thermally buffered populations. We also examine whether improved descriptions of thermal exposure of insect populations can be achieved by combining multiple information sources (i.e., integrating measurements of habitat thermal buffering, habitat thermal amplification, host plant transpiration, and experimental assessments of thermal death time (TDT), thermal avoidance behaviour (TAB) and thermally induced trait plasticity). These integrative analyses are conducted in two demographically declining and two non-declining populations of P. napi. The results show that plastic phenotypic traits (butterfly body mass and wing size) are reliable biomarkers of population vulnerability to extreme thermal conditions. Butterfly wing size is strongly reduced only in thermally exposed populations during summer drought periods. Laboratory rearing of these populations documented reduced wing size due to significant negative effects of increased temperatures affecting larval growth. We conclude that these thermal biomarkers are indicative of the population vulnerability to increasing global warming impacts, showing contrasting trends in thermally exposed and buffered populations. Thermal effects in host plant microsites significantly differ between populations, with stressful thermal conditions only effectively ameliorated in mid-elevation populations. In lowland populations, we observe a sixfold reduction in vegetation thermal buffering effects, and larval growth occurs in these populations at significantly higher temperatures. Lowland populations show reduced host plant quality (C/N ratio), reduced leaf transpiration rates and complete above-ground plant senescence during the peak of summer drought. Amplified host plant temperatures are observed in open microsites, reaching thermal thresholds that can affect larval survival. Overall, our results suggest that butterfly population vulnerability to long-term drought periods is associated with multiple co-occurring and interrelated ecological factors, including limited vegetation thermal buffering effects at lowland sites, significant drought impacts on host plant transpiration and amplified leaf surface temperature, as well as reduced leaf quality linked to the seasonal advance of plant phenology. Our results also identify multiannual summer droughts affecting larval growing periods as a key driver of the recently reported butterfly population declines in the Mediterranean biome.
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3. |
- Leal, Luis, et al.
(author)
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Gene expression profiling across ontogenetic stages in the wood white (Leptidea sinapis) reveals pathways linked to butterfly diapause regulation
- 2018
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In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 27:4, s. 935-948
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Journal article (peer-reviewed)abstract
- 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.
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4. |
- Lukhtanov, Vladimir A., et al.
(author)
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Versatility of multivalent orientation, inverted meiosis, and rescued fitness in holocentric chromosomal hybrids
- 2018
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In: Proceedings of the National Academy of Sciences of the United States of America. - : Proceedings of the National Academy of Sciences. - 0027-8424 .- 1091-6490. ; 115:41, s. E9610-E9619
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Journal article (peer-reviewed)abstract
- 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 F-1 to F-4 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.
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5. |
- Talla, Venkat, et al.
(author)
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Dissecting the Effects of Selection and Mutation on Genetic Diversity in Three Wood White (Leptidea) Butterfly Species
- 2019
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In: Genome Biology and Evolution. - : Oxford University Press. - 1759-6653. ; 11:10, s. 2875-2886
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Journal article (peer-reviewed)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.
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6. |
- Talla, Venkat, et al.
(author)
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Lack of gene flow : Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species
- 2019
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In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 28:16, s. 3756-3770
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Journal article (peer-reviewed)abstract
- 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.
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7. |
- Talla, Venkat, et al.
(author)
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Rapid Increase in Genome Size as a Consequence of Transposable Element Hyperactivity in Wood-White (Leptidea) Butterflies
- 2017
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In: Genome Biology and Evolution. - : Oxford University Press (OUP). - 1759-6653. ; 9:10, s. 2491-2505
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Journal article (peer-reviewed)abstract
- Characterizing and quantifying genome size variation among organisms and understanding if genome size evolves as a consequence of adaptive or stochastic processes have been long-standing goals in evolutionary biology. Here, we investigate genome size variation and association with transposable elements (TEs) across lepidopteran lineages using a novel genome assembly of the common wood-white (Leptidea sinapis) and population re-sequencing data from both L. sinapis and the closely related L. reali and L. juvernica together with 12 previously available lepidopteran genome assemblies. A phylogenetic analysis confirms established relationships among species, but identifies previously unknown intraspecific structure within Leptidea lineages. The genome assembly of L. sinapis is one of the largest of any lepidopteran taxon so far (643Mb) and genome size is correlated with abundance of TEs, both in Lepidoptera in general and within Leptidea where L. juvernica from Kazakhstan has considerably larger genome size than any other Leptidea population. Specific TE subclasses have been active in different Lepidoptera lineages with a pronounced expansion of predominantly LINEs, DNA elements, and unclassified TEs in the Leptidea lineage after the split from other Pieridae. The rate of genome expansion in Leptidea in general has been in the range of four Mb/Million year (My), with an increase in a particular L. juvernica population to 72Mb/My. The considerable differences in accumulation rates of specific TE classes in different lineages indicate that TE activity plays a major role in genome size evolution in butterflies and moths.
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8. |
- Voda, Raluca, et al.
(author)
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Cryptic matters : overlooked species generate most butterfly beta-diversity
- 2015
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In: Ecography. - : Wiley. - 0906-7590 .- 1600-0587. ; 38:4, s. 405-409
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Journal article (peer-reviewed)abstract
- The cryptic fraction of biodiversity is composed of morphologically similar species that are or have been overlooked by scientists. Although current research is increasingly documenting new cases, cryptic species are frequently ignored in large-scale studies and monitoring programs, either because they have not yet been discovered, or because of the practical difficulties involved in differentiating them. However, it is unknown if this could represent a bias extending beyond the number of missed species. By analyzing the butterfly fauna of the west Mediterranean (335 species), we defined cryptic species based on the current consensus of the scientific community, compared their properties to other congeneric species and investigated the consequences of their inclusion/exclusion in beta-diversity analyses. We show that, as defined, the cryptic fraction of butterfly diversity represents about 25% of the west Mediterranean fauna and is overwhelmingly composed by groups of species that are not sympatric. Our results show that co-occurrence among cryptic species is significantly lower than among congeneric non-cryptic species. Accordingly, albeit the frequency of cryptic species is homogenously distributed over the study area, their distribution pattern accounts for most beta-diversity turnover over sea (from 50 to 100%). Beta-diversity turnover, a direct measure of the frequency of species replacement from site to site, is recognized as a fundamental parameter in ecology and is widely used to detect biogeographic patterns. These findings represent a change of paradigm in showing that cryptic diversity comprises original qualitative aspects in addition to merely quantitative ones. This highlights the importance of differentiating cryptic species for various research fields and opens the door to the study of further potential particularities of cryptic diversity.
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9. |
- Wiemers, Martin, et al.
(author)
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An updated checklist of the European Butterflies (Lepidoptera, Papilionoidea)
- 2018
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In: ZooKeys. - : Pensoft Publishers. - 1313-2989 .- 1313-2970. ; 811, s. 9-45
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Journal article (peer-reviewed)abstract
- This paper presents an updated checklist of the butterflies of Europe, together with their original name combinations, and their occurrence status in each European country. According to this checklist, 496 species of the superfamily Papilionoidea occur in Europe. Changes in comparison with the last version (2.6.2) of Fauna Europaea are discussed. Compared to that version, 16 species are new additions, either due to cryptic species most of which have been discovered by molecular methods (13 cases) or due to discoveries of Asian species on the eastern border of the European territory in the Ural mountains (three cases). On the other hand, nine species had to be removed from the list, because they either do not occur in Europe or lost their species status due to new evidence. In addition, three species names had to be changed and 30 species changed their combination due to new evidence on phylogenetic relationships. Furthermore, minor corrections were applied to some authors' names and years of publication. Finally, the name Polyommatusottomanus Lefèbvre, 1831, which is threatened by its senior synonym Lycaenalegeri Freyer, 1830, is declared a nomen protectum, thereby conserving its name in the current combination Lycaenaottomana.
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