West-Eberhard, M. J. Developmental plasticity and evolution. (Oxford University Press, 2003).
de Jong, G. Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. N. Phytologist 166, 101–118 (2005).
Ezard, T. H. G., Prizak, R. & Hoyle, R. B. The fitness costs of adaptation via phenotypic plasticity and maternal effects. Funct. Ecol. 28, 693–701 (2014).
Williams, C. M. et al. Understanding evolutionary impacts of seasonality: an introduction to the symposium. Integr. Comp. Biol. 57, 921–933 (2017).
Google Scholar
Murren, C. J. et al. Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115, 293–301 (2015).
Google Scholar
Sommer, R. J. Phenotypic plasticity: from theory and genetics to current and future challenges. Genetics 215, 1–13 (2020).
Google Scholar
Beldade, P., Mateus, A. R. A. & Keller, R. A. Evolution and molecular mechanisms of adaptive developmental plasticity. Mol. Ecol. 20, 1347–1363 (2011).
Google Scholar
Lafuente, E. & Beldade, P. Genomics of developmental plasticity in animals. Front. Genet. 10, (2019).
Marden, J. H. Quantitative and evolutionary biology of alternative splicing: how changing the mix of alternative transcripts affects phenotypic plasticity and reaction norms. Heredity 100, 111–120 (2008).
Google Scholar
Baralle, F. E. & Giudice, J. Alternative splicing as a regulator of development and tissue identity. Nat. Rev. Mol. Cell Biol. 18, 437–451 (2017).
Google Scholar
Bush, S. J., Chen, L., Tovar-Corona, J. M. & Urrutia, A. O. Alternative splicing and the evolution of phenotypic novelty. Philos. Trans. R. Soc. B: Biol. Sci. 372, 20150474 (2017).
Marden, J. H. & Cobb, J. R. Territorial and mating success of dragonflies that vary in muscle power output and presence of gregarine gut parasites. Anim. Behav. 68, 857–865 (2004).
Kijimoto, T., Moczek, A. P. & Andrews, J. Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns. Proc. Natl Acad. Sci. USA 109, 20526–20531 (2012).
Google Scholar
Bear, A., Prudic, K. L. & Monteiro, A. Steroid hormone signaling during development has a latent effect on adult male sexual behavior in the butterfly Bicyclus anynana. PLoS ONE 12, e0174403 (2017).
Google Scholar
Martin Anduaga, A. et al. Thermosensitive alternative splicing senses and mediates temperature adaptation in Drosophila. eLife 8, e44642 (2019).
Google Scholar
Deshmukh, R., Lakhe, D. & Kunte, K. Tissue-specific developmental regulation and isoform usage underlie the role of doublesex in sex differentiation and mimicry in Papilio swallowtails. R. Soc. Open Sci. 7, 200792 (2020).
Google Scholar
Grantham, M. E. & Brisson, J. A. Extensive differential splicing underlies phenotypically plastic aphid morphs. Mol. Biol. Evol. 35, 1934–1946 (2018).
Google Scholar
Price, J. et al. Alternative splicing associated with phenotypic plasticity in the bumble bee Bombus terrestris. Mol. Ecol. 27, 1036–1043 (2018).
Google Scholar
Lees, J. G., Ranea, J. A. & Orengo, C. A. Identifying and characterising key alternative splicing events in Drosophila development. BMC Genomics 16, 608 (2015).
Google Scholar
Jakšić, A. M. & Schlötterer, C. The interplay of temperature and genotype on patterns of alternative splicing in Drosophila melanogaster. Genetics 204, 315–325 (2016).
Google Scholar
Healy, T. M. & Schulte, P. M. Patterns of alternative splicing in response to cold acclimation in fish. J. Exp. Biol. 222, jeb193516 (2019).
Signor, S. & Nuzhdin, S. Dynamic changes in gene expression and alternative splicing mediate the response to acute alcohol exposure in Drosophila melanogaster. Heredity 121, 342–360 (2018).
Google Scholar
Lang, A. S., Austin, S. H., Harris, R. M., Calisi, R. M. & MacManes, M. D. Stress-mediated convergence of splicing landscapes in male and female rock doves. BMC Genomics 21, 251 (2020).
Google Scholar
Suresh, S., Crease, T. J., Cristescu, M. E. & Chain, F. J. J. Alternative splicing is highly variable among Daphnia pulex lineages in response to acute copper exposure. BMC Genomics 21, 433 (2020).
Google Scholar
Thorstensen, M. J., Baerwald, M. R. & Jeffries, K. M. RNA sequencing describes both population structure and plasticity-selection dynamics in a non-model fish. BMC Genomics 22, 273 (2021).
Google Scholar
Singh, A. & Agrawal, A. F. Sexual dimorphism in gene expression: coincidence and population genomics of two forms of differential expression in Drosophila melanogaster. bioRxiv (2021) https://doi.org/10.1101/2021.02.08.429268.
Rogers, T. F., Palmer, D. H. & Wright, A. E. Sex-specific selection drives the evolution of alternative splicing in birds. Mol. Biol. Evolution 38, 519–530 (2021).
Google Scholar
Fox, R. J., Donelson, J. M., Schunter, C., Ravasi, T. & Gaitán-Espitia, J. D. Beyond buying time: the role of plasticity in phenotypic adaptation to rapid environmental change. Philos. Trans. R. Soc. B: Biol. Sci. 374, 20180174 (2019).
Kelly, M. Adaptation to climate change through genetic accommodation and assimilation of plastic phenotypes. Philos. Trans. R. Soc. B: Biol. Sci. 374, 20180176 (2019).
Oostra, V., Saastamoinen, M., Zwaan, B. J. & Wheat, C. W. Strong phenotypic plasticity limits potential for evolutionary responses to climate change. Nat. Commun. 9, 1–11 (2018).
Google Scholar
Wang, Y. et al. Mechanism of alternative splicing and its regulation (Review). Biomed. Rep. 3, 152–158 (2015).
Google Scholar
Ule, J. & Blencowe, B. J. Alternative splicing regulatory networks: functions, mechanisms, and evolution. Mol. Cell 76, 329–345 (2019).
Google Scholar
McManus, C. J., Coolon, J. D., Eipper-Mains, J., Wittkopp, P. J. & Graveley, B. R. Evolution of splicing regulatory networks in Drosophila. Genome Res. 24, 786–796 (2014).
Google Scholar
Gao, Q., Sun, W., Ballegeer, M., Libert, C. & Chen, W. Predominant contribution of cis-regulatory divergence in the evolution of mouse alternative splicing. Mol. Syst. Biol. 11, 816 (2015).
Google Scholar
Barbosa-Morais, N. L. et al. The evolutionary landscape of alternative splicing in vertebrate species. Science 338, 1587–1593 (2012).
Google Scholar
Wang, X. et al. Cis-regulated alternative splicing divergence and its potential contribution to environmental responses in Arabidopsis. Plant J. 97, 555–570 (2019).
Google Scholar
Huang, Y., Lack, J. B., Hoppel, G. T. & Pool, J. E. Parallel and population-specific gene regulatory evolution in cold-adapted fly populations. bioRxiv (2021) https://doi.org/10.1101/795716.
Lewis, J. J., Van Belleghem, S. M., Papa, R., Danko, C. G. & Reed, R. D. Many functionally connected loci foster adaptive diversification along a neotropical hybrid zone. Sci. Adv. 6, eabb8617 (2020).
Google Scholar
Lewis, J. J. & Reed, R. D. Genome-wide regulatory adaptation shapes population-level genomic landscapes in Heliconius. Mol. Biol. Evol. 36, 159–173 (2019).
Google Scholar
Martin, S. H. et al. Natural selection and genetic diversity in the butterfly Heliconius melpomene. Genetics 203, 525–541 (2016).
Google Scholar
Brakefield, P. M., Beldade, P. & Zwaan, B. J. The African Butterfly Bicyclus anynana: a model for evolutionary genetics and evolutionary developmental biology. Cold Spring Harb. Protoc. 2009, pdb.emo122 (2009).
Google Scholar
Mateus, A. R. A. et al. Adaptive developmental plasticity: compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility. BMC Biol. 12, 97 (2014).
Google Scholar
Oostra, V. et al. Ecdysteroid hormones link the juvenile environment to alternative adult life histories in a seasonal insect. Am. Naturalist 184, E79–E92 (2014).
van Bergen, E. et al. Conserved patterns of integrated developmental plasticity in a group of polyphenic tropical butterflies. BMC Evolut. Biol. 17, 59 (2017).
Singh, P. et al. Complex multi-trait responses to multivariate environmental cues in a seasonal butterfly. Evol. Ecol. (2020) https://doi.org/10.1007/s10682-020-10062-0.
Prudic, K. L., Jeon, C., Cao, H. & Monteiro, A. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation. Science 331, 73–75 (2011).
Google Scholar
Chen, L., Bush, S. J., Tovar-Corona, J. M., Castillo-Morales, A. & Urrutia, A. O. Correcting for differential transcript coverage reveals a strong relationship between alternative splicing and organism complexity. Mol. Biol. Evol. 31, 1402–1413 (2014).
Google Scholar
Hamid, F. M. & Makeyev, E. V. Emerging functions of alternative splicing coupled with nonsense-mediated decay. Biochem. Soc. Trans. 42, 1168–1173 (2014).
Google Scholar
Tabrez, S. S., Sharma, R. D., Jain, V., Siddiqui, A. A. & Mukhopadhyay, A. Differential alternative splicing coupled to nonsense-mediated decay of mRNA ensures dietary restriction-induced longevity. Nat. Commun. 8, 306 (2017).
Google Scholar
Uller, T., Moczek, A. P., Watson, R. A., Brakefield, P. M. & Laland, K. N. Developmental bias and evolution: a regulatory network perspective. Genetics 209, 949–966 (2018).
Google Scholar
Nijhout, H. F. To plasticity and back again. eLife 4, e06995 (2015).
Google Scholar
Helanterä, H. & Uller, T. Neutral and adaptive explanations for an association between caste-biased gene expression and rate of sequence evolution. Front. Genet. 5, 297 (2014).
Pespeni, M. H., Ladner, J. T. & Moczek, A. P. Signals of selection in conditionally expressed genes in the diversification of three horned beetle species. J. Evolut. Biol. 30, 1644–1657 (2017).
Google Scholar
Plass, M. & Eyras, E. Differentiated evolutionary rates in alternative exons and the implications for splicing regulation. BMC Evol. Biol. 6, 50 (2006).
Google Scholar
Chen, F.-C., Pan, C.-L. & Lin, H.-Y. Independent effects of alternative splicing and structural constraint on the evolution of mammalian coding exons. Mol. Biol. Evolution 29, 187–193 (2012).
Google Scholar
Peña, C., Nylin, S. & Wahlberg, N. The radiation of Satyrini butterflies (Nymphalidae: Satyrinae): a challenge for phylogenetic methods. Zool. J. Linn. Soc. 161, 64–87 (2011).
Bhardwaj, S. et al. Origin of the mechanism of phenotypic plasticity in satyrid butterfly eyespots. eLife 9, e49544 (2020).
Google Scholar
Lewis, B. P., Green, R. E. & Brenner, S. E. Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. PNAS 100, 189–192 (2003).
Google Scholar
Akerman, M. & Mandel-Gutfreund, Y. Alternative splicing regulation at tandem 3′ splice sites. Nucleic Acids Res. 34, 23–31 (2006).
Google Scholar
Moran, N. A. The evolutionary maintenance of alternative phenotypes. Am. Naturalist 139, 971–989 (1992).
Nijhout, H. F. Development and evolution of adaptive polyphenisms. Evolution Dev. 5, 9–18 (2003).
Mank, J. E. The transcriptional architecture of phenotypic dimorphism. Nat. Ecol. Evolution 1, 1–7 (2017).
Scheiner, S. M., Barfield, M. & Holt, R. D. The genetics of phenotypic plasticity. XVII. Response to climate change. Evolut. Appl. 13, 388–399 (2020).
Osada, N., Miyagi, R. & Takahashi, A. Cis- and trans-regulatory effects on gene expression in a natural population of Drosophila melanogaster. Genetics 206, 2139–2148 (2017).
Google Scholar
Cooper, R. D. & Shaffer, H. B. Allele-specific expression and gene regulation help explain transgressive thermal tolerance in non-native hybrids of the endangered California tiger salamander (Ambystoma californiense). Mol. Ecol. 30, 987–1004 (2021).
Google Scholar
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
Google Scholar
Baruzzo, G. et al. Simulation-based comprehensive benchmarking of RNA-seq aligners. Nat. Methods 14, 135–139 (2017).
Google Scholar
Schuierer, S. et al. A comprehensive assessment of RNA-seq protocols for degraded and low-quantity samples. BMC Genomics 18, 442 (2017).
Google Scholar
Broad Institute. Picard toolkit. (2019).
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
Google Scholar
Liao, Y., Smyth, G. K. & Shi, W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res 47, e47–e47 (2019).
Google Scholar
Chen, Y., Lun, A. T. L. & Smyth, G. K. From reads to genes to pathways: differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Res 5, 1438 (2016).
Google Scholar
R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2019).
Shen, L. GeneOverlap: Test and visualize gene overlaps. (2020).
Gu, Z., Eils, R. & Schlesner, M. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics 32, 2847–2849 (2016).
Google Scholar
Huerta-Cepas, J. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47, D309–D314 (2019).
Google Scholar
Alexa, A. & Rahnenfuhrer, J. topGO: Enrichment analysis for Gene Ontology. (2016).
Larsson, J. et al. eulerr: Area-Proportional Euler and Venn Diagrams with Ellipses. (2021).
Supek, F., Bošnjak, M., Škunca, N. & Šmuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800 (2011).
Google Scholar
Gu, Z. & Hübschmann, D. simplifyEnrichment: an R/Bioconductor package for Clustering and Visualizing Functional Enrichment Results. 2020.10.27.312116 (2020) https://doi.org/10.1101/2020.10.27.312116.
Gu, Z. simplifyEnrichment: Simplify Functional Enrichment Results. (Bioconductor version: Release (3.13), 2021). https://doi.org/10.18129/B9.bioc.simplifyEnrichment.
de Jong, M. A., Wahlberg, N., Eijk, M., van, Brakefield, P. M. & Zwaan, B. J. Mitochondrial DNA signature for range-wide populations of Bicyclus anynana suggests a rapid expansion from recent Refugia. PLoS ONE 6, e21385 (2011).
Google Scholar
de Jong, M. A., Collins, S., Beldade, P., Brakefield, P. M. & Zwaan, B. J. Footprints of selection in wild populations of Bicyclus anynana along a latitudinal cline. Mol. Ecol. 22, 341–353 (2013).
Google Scholar
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 10–12 (2011).
Joshi, N. & Fass, J. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files.
Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997 [q-bio] (2013).
Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: analysis of next generation sequencing data. BMC Bioinforma. 15, 356 (2014).
Nowell, R. W. et al. A high-coverage draft genome of the mycalesine butterfly Bicyclus anynana. GigaScience 6, (2017).
Xu, L. et al. OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Res. 47, W52–W58 (2019).
Google Scholar
Ranwez, V., Harispe, S., Delsuc, F. & Douzery, E. J. P. MACSE: multiple alignment of coding SEquences accounting for frameshifts and stop codons. PLoS ONE 6, e22594 (2011).
Google Scholar
Lucaci, A. G., Wisotsky, S. R., Shank, S. D., Weaver, S. & Kosakovsky Pond, S. L. Extra base hits: widespread empirical support for instantaneous multiple-nucleotide changes. PLoS One 16, e0248337 (2021).
Google Scholar
Buerkner, P.-C. brms: An R Package for Bayesian Multilevel Models Using Stan. J. Stat. Softw. 80, 1–28 (2017).
Buerkner, P.-C. Advanced Bayesian multilevel modeling with the R Package brms. R. J. 10, 395–411 (2018).
Kassambara, A. rstatix: Pipe-Friendly Framework for Basic Statistical Tests. (2021).
Shen, S. et al. rMATS: Robust and flexible detection of differential alternative splicing from replicate RNA-Seq data. Proc. Natl Acad. Sci. USA 111, E5593–E5601 (2014).
Google Scholar
Alamancos, G. P., Pagès, A., Trincado, J. L., Bellora, N. & Eyras, E. Leveraging transcript quantification for fast computation of alternative splicing profiles. RNA 21, 1521–1531 (2015).
Google Scholar
Wang, Q. & Rio, D. C. JUM is a computational method for comprehensive annotation-free analysis of alternative pre-mRNA splicing patterns. Proc. Natl Acad. Sci. USA115, E8181–E8190 (2018).
Google Scholar
Wickham, H. et al. Welcome to the Tidyverse. J. Open Source Softw. 4, 1686 (2019).
Google Scholar
Kassambara, A. ggpubr” ‘ggplot2’ based publication-ready plots. (2020).
Bivand, R. & Rundel, C. rgeos: Interface to Geometry Engine – Open Source (‘GEOS’). (2021).
South, A. afrilearndata: Small Africa Map Datasets for Learning. (2021).
Inkscape Project. Inkscape. (2021).
Steward, R. A., Oostra, V. & Wheat, C. W. B_anynana_differentialSplicing Github. zenodo.org https://zenodo.org/badge/latestdoi/255903232 (2021).
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