Does the definition of a novel environment affect the ability to detect cryptic genetic variation?

Anthropogenic change exposes populations to environments that have been rare or entirely absent from their evolutionary past. Such novel environments are hypothesized to release cryptic genetic variation, a hidden store of variance that can fuel evolution. However, support for this hypothesis is mixed. One possible reason is a lack of clarity in what is meant by 'novel environment', an umbrella term encompassing conditions with potentially contrasting effects on the exposure or concealment of cryptic variation. Here, we use a meta-analysis approach to investigate changes in the total genetic variance of multivariate traits in ancestral versus novel environments. To determine whether the definition of a novel environment could explain the mixed support for a release of cryptic genetic variation, we compared absolute novel environments, those not represented in a population's evolutionary past, to extreme novel environments, those involving frequency or magnitude changes to environments present in a population's ancestry. Despite sufficient statistical power, we detected no broad-scale pattern of increased genetic variance in novel environments, and finding the type of novel environment did not explain any significant variation in effect sizes. When effect sizes were partitioned by experimental design, we found increased genetic variation in studies based on broad-sense measures of variance, and decreased variation in narrow-sense studies, in support of previous research. Therefore, the source of genetic variance, not the definition of a novel environment, was key to understanding environment-dependant genetic variation, highlighting non-additive genetic variance as an important component of cryptic genetic variation and avenue for future research.

Digest: Habitat seasonality drives evolutionary change in plasticity in Bicyclus butterflies.

Can changes in plasticity evolve in populations in response to local conditions? Zhen et al. addressed this question using populations of Bicyclus butterflies from Cameroon. The results of the study suggest that local adaptation in these African butterflies involved changes in the degree of plasticity, such that stronger responses to temperature were found in populations from habitats with stronger seasonal fluctuations. Interestingly, differentiation in reaction norms occurred despite high levels of gene flow among populations, indicating a small number of loci contributing to evolved differences in plasticity.

Alternative splicing in seasonal plasticity and the potential for adaptation to environmental change.

Seasonal plasticity is accomplished via tightly regulated developmental cascades that translate environmental cues into trait changes. Little is known about how alternative splicing and other posttranscriptional molecular mechanisms contribute to plasticity or how these mechanisms impact how plasticity evolves. Here, we use transcriptomic and genomic data from the butterfly Bicyclus anynana, a model system for seasonal plasticity, to compare the extent of differential expression and splicing and test how these axes of transcriptional plasticity differ in their potential for evolutionary change. Between seasonal morphs, we find that differential splicing affects a smaller but functionally unique set of genes compared to differential expression. Further, we find strong support for the novel hypothesis that spliced genes are more susceptible than differentially expressed genes to erosion of genetic variation due to selection on seasonal plasticity. Our results suggest that splicing plasticity is especially likely to experience genetic constraints that could affect the potential of wild populations to respond to rapidly changing environments.

Improved chromosome-level genome assembly of the Glanville fritillary butterfly (Melitaea cinxia) integrating Pacific Biosciences long reads and a high-density linkage map.

BACKGROUND: The Glanville fritillary (Melitaea cinxia) butterfly is a model system for metapopulation dynamics research in fragmented landscapes. Here, we provide a chromosome-level assembly of the butterfly's genome produced from Pacific Biosciences sequencing of a pool of males, combined with a linkage map from population crosses. RESULTS: The final assembly size of 484 Mb is an increase of 94 Mb on the previously published genome. Estimation of the completeness of the genome with BUSCO indicates that the genome contains 92-94% of the BUSCO genes in complete and single copies. We predicted 14,810 genes using the MAKER pipeline and manually curated 1,232 of these gene models. CONCLUSIONS: The genome and its annotated gene models are a valuable resource for future comparative genomics, molecular biology, transcriptome, and genetics studies on this species.

Alternative developmental and transcriptomic responses to host plant water limitation in a butterfly metapopulation.

Predicting how climate change affects biotic interactions poses a challenge. Plant-insect herbivore interactions are particularly sensitive to climate change, as climate-induced changes in plant quality cascade into the performance of insect herbivores. Whereas the immediate survival of herbivore individuals depends on plastic responses to climate change-induced nutritional stress, long-term population persistence via evolutionary adaptation requires genetic variation for these responses. To assess the prospects for population persistence under climate change, it is therefore crucial to characterize response mechanisms to climate change-induced stressors, and quantify their variability in natural populations. Here, we test developmental and transcriptomic responses to water limitation-induced host plant quality change in a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We combine nuclear magnetic resonance spectroscopy on the plant metabolome, larval developmental assays and an RNA sequencing analysis of the larval transcriptome. We observed that responses to feeding on water-limited plants, in which amino acids and aromatic compounds are enriched, showed marked variation within the metapopulation, with individuals of some families performing better on control and others on water-limited plants. The transcriptomic responses were concordant with the developmental responses: families exhibiting opposite developmental responses also produced opposite transcriptomic responses (e.g. in growth-associated transcripts). The divergent responses in both larval development and transcriptome are associated with differences between families in amino acid catabolism and storage protein production. The results reveal intrapopulation variability in plasticity, suggesting that the Finnish M. cinxia metapopulation harbours potential for buffering against drought-induced changes in host plant quality.

Effects of adult temperature on gene expression in a butterfly: identifying pathways associated with thermal acclimation.

BACKGROUND: Phenotypic plasticity is a pervasive property of all organisms and considered to be of key importance for dealing with environmental variation. Plastic responses to temperature, which is one of the most important ecological factors, have received much attention over recent decades. A recurrent pattern of temperature-induced adaptive plasticity includes increased heat tolerance after exposure to warmer temperatures and increased cold tolerance after exposure to cooler temperatures. However, the mechanisms underlying these plastic responses are hitherto not well understood. Therefore, we here investigate effects of adult acclimation on gene expression in the tropical butterfly Bicyclus anynana, using an RNAseq approach. RESULTS: We show that several antioxidant markers (e.g. peroxidase, cytochrome P450) were up-regulated at a higher temperature compared with a lower adult temperature, which might play an important role in the acclamatory responses subsequently providing increased heat tolerance. Furthermore, several metabolic pathways were up-regulated at the higher temperature, likely reflecting increased metabolic rates. In contrast, we found no evidence for a decisive role of the heat shock response. CONCLUSIONS: Although the important role of antioxidant defence mechanisms in alleviating detrimental effects of oxidative stress is firmly established, we speculate that its potentially important role in mediating heat tolerance and survival under stress has been underestimated thus far and thus deserves more attention.

Research priorities for maintaining biodiversity's contributions to people in Latin America.

Maintaining biodiversity is crucial for ensuring human well-being. The authors participated in a workshop held in Palenque, Mexico, in August 2018, that brought together 30 mostly early-career scientists working in different disciplines (natural, social and economic sciences) with the aim of identifying research priorities for studying the contributions of biodiversity to people and how these contributions might be impacted by environmental change. Five main groups of questions emerged: (1) Enhancing the quantity, quality, and availability of biodiversity data; (2) Integrating different knowledge systems; (3) Improved methods for integrating diverse data; (4) Fundamental questions in ecology and evolution; and (5) Multi-level governance across boundaries. We discuss the need for increased capacity building and investment in research programmes to address these challenges.

Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis.

BACKGROUND: Selection acts on the phenotype, yet only the genotype is inherited. While both the phenotypic and genotypic response to short-term selection can be measured, the link between these is a major unsolved problem in evolutionary biology, in particular for complex behavioural phenotypes. RESULTS: Here we characterize the genomic and the transcriptomic basis of associative learning ability in the parasitic wasp Nasonia vitripennis and use gene network analysis to link the two. We artificially selected for improved associative learning ability in four independent pairs of lines and identified signatures of selection across the genome. Allele frequency diverged consistently between the selected and control lines in 118 single nucleotide polymorphisms (SNPs), clustering in 51 distinct genomic regions containing 128 genes. The majority of SNPs were found in regulatory regions, suggesting a potential role for gene expression evolution. We therefore sequenced the transcriptomes of selected and control lines and identified 36 consistently differentially expressed transcripts with large changes in expression. None of the differentially expressed genes also showed sequence divergence as a result of selection. Instead, gene network analysis showed many of the genes with consistent allele frequency differences and all of the differentially expressed genes to cluster in a single co-expression network. At a functional level, both genomic and transcriptomic analyses implicated members of gene networks known to be involved in neural plasticity and cognitive processes. CONCLUSIONS: Taken together, our results reveal how specific cognitive abilities can readily respond to selection via a complex interplay between regulatory and sequence evolution.

Strong phenotypic plasticity limits potential for evolutionary responses to climate change.

Phenotypic plasticity, the expression of multiple phenotypes from one genome, is a widespread adaptation to short-term environmental fluctuations, but whether it facilitates evolutionary adaptation to climate change remains contentious. Here, we investigate seasonal plasticity and adaptive potential in an Afrotropical butterfly expressing distinct phenotypes in dry and wet seasons. We assess the transcriptional architecture of plasticity in a full-factorial analysis of heritable and environmental effects across 72 individuals, and reveal pervasive gene expression differences between the seasonal phenotypes. Strikingly, intra-population genetic variation for plasticity is largely absent, consistent with specialisation to a particular environmental cue reliably predicting seasonal transitions. Under climate change, deteriorating accuracy of predictive cues will likely aggravate maladaptive phenotype-environment mismatches and increase selective pressures on reaction norms. However, the observed paucity of genetic variation for plasticity limits evolutionary responses, potentially weakening prospects for population persistence. Thus, seasonally plastic species may be especially vulnerable to climate change.

A high-coverage draft genome of the mycalesine butterfly Bicyclus anynana.

The mycalesine butterfly Bicyclus anynana, the "Squinting bush brown," is a model organism in the study of lepidopteran ecology, development, and evolution. Here, we present a draft genome sequence for B. anynana to serve as a genomics resource for current and future studies of this important model species. Seven libraries with insert sizes ranging from 350 bp to 20 kb were constructed using DNA from an inbred female and sequenced using both Illumina and PacBio technology; 128 Gb of raw Illumina data was filtered to 124 Gb and assembled to a final size of 475 Mb (∼×260 assembly coverage). Contigs were scaffolded using mate-pair, transcriptome, and PacBio data into 10 800 sequences with an N50 of 638 kb (longest scaffold 5 Mb). The genome is comprised of 26% repetitive elements and encodes a total of 22 642 predicted protein-coding genes. Recovery of a BUSCO set of core metazoan genes was almost complete (98%). Overall, these metrics compare well with other recently published lepidopteran genomes. We report a high-quality draft genome sequence for Bicyclus anynana. The genome assembly and annotated gene models are available at LepBase (http://ensembl.lepbase.org/index.html).

Convergent recombination suppression suggests role of sexual selection in guppy sex chromosome formation.

Sex chromosomes evolve once recombination is halted between a homologous pair of chromosomes. The dominant model of sex chromosome evolution posits that recombination is suppressed between emerging X and Y chromosomes in order to resolve sexual conflict. Here we test this model using whole genome and transcriptome resequencing data in the guppy, a model for sexual selection with many Y-linked colour traits. We show that although the nascent Y chromosome encompasses nearly half of the linkage group, there has been no perceptible degradation of Y chromosome gene content or activity. Using replicate wild populations with differing levels of sexually antagonistic selection for colour, we also show that sexual selection leads to greater expansion of the non-recombining region and increased Y chromosome divergence. These results provide empirical support for longstanding models of sex chromosome catalysis, and suggest an important role for sexual selection and sexual conflict in genome evolution.

Adaptive developmental plasticity: compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility.

BACKGROUND: The environmental regulation of development can result in the production of distinct phenotypes from the same genotype and provide the means for organisms to cope with environmental heterogeneity. The effect of the environment on developmental outcomes is typically mediated by hormonal signals which convey information about external cues to the developing tissues. While such plasticity is a wide-spread property of development, not all developing tissues are equally plastic. To understand how organisms integrate environmental input into coherent adult phenotypes, we must know how different body parts respond, independently or in concert, to external cues and to the corresponding internal signals. RESULTS: We quantified the effect of temperature and ecdysone hormone manipulations on post-growth tissue patterning in an experimental model of adaptive developmental plasticity, the butterfly Bicyclus anynana. Following a suite of traits evolving by natural or sexual selection, we found that different groups of cells within the same tissue have sensitivities and patterns of response that are surprisingly distinct for the external environmental cue and for the internal hormonal signal. All but those wing traits presumably involved in mate choice responded to developmental temperature and, of those, all but the wing traits not exposed to predators responded to hormone manipulations. On the other hand, while patterns of significant response to temperature contrasted traits on autonomously-developing wings, significant response to hormone manipulations contrasted neighboring groups of cells with distinct color fates. We also showed that the spatial compartmentalization of these responses cannot be explained by the spatial or temporal compartmentalization of the hormone receptor protein. CONCLUSIONS: Our results unravel the integration of different aspects of the adult phenotype into developmental and functional units which both reflect and impact evolutionary change. Importantly, our findings underscore the complexity of the interactions between environment and physiology in shaping the development of different body parts.

On the fate of seasonally plastic traits in a rainforest butterfly under relaxed selection.

Many organisms display phenotypic plasticity as adaptation to seasonal environmental fluctuations. Often, such seasonal responses entails plasticity of a whole suite of morphological and life-history traits that together contribute to the adaptive phenotypes in the alternative environments. While phenotypic plasticity in general is a well-studied phenomenon, little is known about the evolutionary fate of plastic responses if natural selection on plasticity is relaxed. Here, we study whether the presumed ancestral seasonal plasticity of the rainforest butterfly Bicyclus sanaos (Fabricius, 1793) is still retained despite the fact that this species inhabits an environmentally stable habitat. Being exposed to an atypical range of temperatures in the laboratory revealed hidden reaction norms for several traits, including wing pattern. In contrast, reproductive body allocation has lost the plastic response. In the savannah butterfly, B. anynana (Butler, 1879), these traits show strong developmental plasticity as an adaptation to the contrasting environments of its seasonal habitat and they are coordinated via a common developmental hormonal system. Our results for B. sanaos indicate that such integration of plastic traits - as a result of past selection on expressing a coordinated environmental response - can be broken when the optimal reaction norms for those traits diverge in a new environment.

Ecdysteroid hormones link the juvenile environment to alternative adult life histories in a seasonal insect.

The conditional expression of alternative life strategies is a widespread feature of animal life and a pivotal adaptation to life in seasonal environments. To optimally match suites of traits to seasonally changing ecological opportunities, animals living in seasonal environments need mechanisms linking information on environmental quality to resource allocation decisions. The butterfly Bicyclus anynana expresses alternative adult life histories in the alternating wet and dry seasons of its habitat as endpoints of divergent developmental pathways triggered by seasonal variation in preadult temperature. Pupal ecdysteroid hormone titers are correlated with the seasonal environment, but whether they play a functional role in coordinating the coupling of adult traits in the alternative life histories is unknown. Here, we show that manipulating pupal ecdysteroid levels is sufficient to mimic in direction and magnitude the shifts in adult reproductive resource allocation normally induced by seasonal temperature. Crucially, this allocation shift is accompanied by changes in ecologically relevant traits, including timing of reproduction, life span, and starvation resistance. Together, our results support a functional role for ecdysteroids during development in mediating strategic reproductive investment decisions in response to predictive indicators of environmental quality. This study provides a physiological mechanism for adaptive developmental plasticity, allowing organisms to cope with variable environments.

Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly.

Polyphenisms-the expression of discrete phenotypic morphs in response to environmental variation-are examples of phenotypic plasticity that may potentially be adaptive in the face of predictable environmental heterogeneity. In the butterfly Bicyclus anynana, we examine the hormonal regulation of phenotypic plasticity that involves divergent developmental trajectories into distinct adult morphs for a suite of traits as an adaptation to contrasting seasonal environments. This polyphenism is induced by temperature during development and mediated by ecdysteroid hormones. We reared larvae at separate temperatures spanning the natural range of seasonal environments and measured reaction norms for ecdysteroids, juvenile hormones (JHs) and adult fitness traits. Timing of peak ecdysteroid, but not JH titres, showed a binary response to the linear temperature gradient. Several adult traits (e.g. relative abdomen mass) responded in a similar, dimorphic manner, while others (e.g. wing pattern) showed a linear response. This study demonstrates that hormone dynamics can translate a linear environmental gradient into a discrete signal and, thus, that polyphenic differences between adult morphs can already be programmed at the stage of hormone signalling during development. The range of phenotypic responses observed within the suite of traits indicates both shared regulation and independent, trait-specific sensitivity to the hormone signal.