Anna Runemark

Land-use change driven by agricultural intensification is a major contributor to insect declines globally. As a result of population decline and subdivision, species lose genetic diversity, reducing adaptive potential and increasing genetic load. We examine how genetic diversity has changed over the past century in three focal and five additional Polyommatinae butterfly species in Sweden by sequencing specimens from museum collections. Based on 59 historical and 90 contemporary genomes, we document a 6% decline in heterozygosity in the grassland specialist Cyaniris semiargus, driven by division into small, isolated populations. In contrast, generalist Polyommatus icarus and heathland specialist Plebejus argus have maintained genetic diversity and connectivity. Reduced heterozygosity in Cy. semiargus reflects increases in runs of homozygosity, increasing the homozygosity of derived mutations at missense and conserved positions. While genomic erosion is currently relatively mild, it is expected to lag demographic change. We infer that demographic decline in Cy. semiargus is considerably larger than declines in genetic diversity to date. We use simulations to demonstrate that only mild losses of genetic diversity are expected at the early stages of demographic decline, leaving populations with substantial genetic extinction debt. We detect similar reductions in genetic diversity in two of five additional species, underscoring the need for restoring habitat connectivity and gene flow to limit further genomic erosion in specialist grassland insects. This study illustrates how incorporation of genetic monitoring into conservation planning can identify where demographic decline has left populations with a genetic extinction debt even after they stabilize.

Polyploidization is an important driver of evolution and diversification in flowering plants. Here, we assess how repeated polyploidization may have shaped diversification of floral morphology in Lithophragma bolanderi (Saxifragaceae). This species comprises multiple cytotypes and varies geographically in its interactions with specialized pollinating moths in the genus Greya (Prodoxidae). Past studies have shown that coevolution with these moths has favored particular suites of floral characters but does not fully explain local and regional floral diversification. We combined phenotypic and genomic data from more than 1,800 individuals from 40 L. bolanderi populations spread across its entire range. Flow-cytometric analyses revealed a geographic mosaic of populations comprising one to four of three dominant (diploid, tetraploid, hexaploid) and three rare (triploid, pentaploid, octoploid) cytotypes. Whole-genome resequencing of a subset of populations suggested that polyploids arose from multiple autopolyploidization events, rather than a single event and/or through hybridization, albeit with some signals consistent with low levels of introgression from the congener Lithophragma glabrum . Quantification of flower traits from plants grown in a common garden showed that cytotype explained more than 15% of the variation in floral morphology, with polyploids showing more variability than diploids. Experimental induction of neopolyploids directly induced phenotypic changes but also indicated that local selection may have favored subsequent convergence in floral morphology among cytotypes in natural populations. Collectively, this comprehensive and integrative approach provides insights into how variability generating processes, such as polyploidization integrates with selection from species interactions to shape local floral diversification.

How gene expression evolves to enable divergent ecological adaptation and how changes in gene expression relate to genomic architecture are pressing questions for understanding the mechanisms enabling adaptation and ecological speciation. Furthermore, how plasticity in gene expression can both contribute to and be affected by the process of ecological adaptation is crucial to understanding gene expression evolution, colonisation of novel niches and response to rapid environmental change. Here, we investigate the role of constitutive and plastic gene expression differences between host races, or host‐specific ecotypes, of the peacock fly Tephritis conura, a thistle bud specialist. By cross‐fostering larvae to new buds of their natal host plant or the alternative, novel host plant, we uncover extensive constitutive differences in gene expression between the host races, especially genes associated with processing of host plant chemicals. However, evidence for expression plasticity was minimal and limited to the ancestral host race. Genes with host race‐specific expression are found more often than expected within a large inversion in the T. conura genome, adding to evidence that inversions are important for enabling diversification in the face of gene flow and underscores that altered gene expression may be key to understanding the evolutionary consequences of inversions.

Land-use change from agricultural intensification is a major driver of global insect declines. We investigated the genetic consequences of grassland decline in Sweden by sequencing museum and modern specimens of three focal and five additional Polyommatinae butterfly species. From 59 historical and 90 contemporary genomes, we find a 6% decline in genetic diversity and increased isolation and inbreeding in the grassland specialist Cyaniris semiargus over the past 70 years. In contrast, generalist Polyommatus icarus and heathland specialist Plebejus argus maintained genetic diversity and connectivity. Although currently genomic erosion is mild, we infer it lags considerably larger declines in effective population sizes. Using simulations, we demonstrate that only a small portion of genetic diversity is lost in early stages of decline, creating a genetic extinction debt. Two of five additional species show similar reductions, underscoring that restoration of grassland habitat is necessary to restore gene flow and halt further genomic erosion in grassland insects.

Understanding the evolution of evolvability—the evolutionary potential of populations—is key to predicting adaptation to novel environments. Despite growing evidence that evolvability structures adaptation, it remains unclear how adaptation to novel environments in turn influences evolvability. Here we address the interplay between adaptation and evolvability in the peacock fly Tephritis conura, which recently underwent an adaptive change in ovipositor length following a host shift. We compared the evolvability of morphological traits, including ovipositor length, between the ancestral and the derived host race. We found that mean evolvability was reduced in females of the derived host race compared to the ancestral host race. However, patterns of multivariate evolvability (considering trait covariances) were very similar in both host races, and populations of the derived host race had diverged from the ancestral host race in directions of greater-than-average evolvability. Exploration of phenotypic integration patterns further revealed relatively high levels of independent variation in ovipositor length compared to other measured traits, allowing some degree of independent divergence. Our findings suggest that adaptation to novel environments can reduce mean evolvability without major changes in patterns of variational constraints, and that trait autonomy helps facilitate divergence of functionally important traits.

Gene expression, resulting from complex regulatory interactions, plays an important role in adaptation and speciation. While gene expression historically has been studied in the context of reproductive isolation in speciation research, a role for evolved differences in gene expression in adaptation to novel niches is increasingly appreciated. How gene expression evolves and enables divergent ecological adaptation, and how changes in gene expression relate to genomic architecture and genetic divergence are pressing questions in understanding the processes of adaptation and ecological speciation. Further, how plasticity in gene expression can both contribute to and be affected by the process of ecological adaptation is a crucial component in understanding gene expression evolution. To address these questions, we investigate the role of evolved and plastic gene expression differences in adaptation leveraging an established host plant shift in the peacock fly Tephritis conura . Using a cross-fostering design where larvae feed on either natal or alternate host plants, we uncover extensive evolved differences in gene expression between the ecotypes, strikingly in genes associated with processing of host plant chemicals. We find limited evidence for plasticity, with some indications of higher plasticity in the ancestral ecotype where the expression of three gene coexpression modules is altered when larvae are cross-fostered to the derived host plant. Interestingly, we find an enrichment of differentially expressed genes within a large, ecotype-specific inversion in the T. conura genome. This finding adds to evidence that inversions are important for enabling diversification in the face of gene flow and underscores that effects on gene expression may be key to understanding the role of inversions.

Gene expression has a key role in reproductive isolation, and studies of hybrid gene expression have identified mechanisms causing hybrid sterility. Here, we review the evidence for altered gene expression following hybridization and outline the mechanisms shown to contribute to altered gene expression in hybrids. Transgressive gene expression, transcending that of both parental species, is pervasive in early generation sterile hybrids, but also frequently observed in viable, fertile hybrids. We highlight studies showing that hybridization can result in transgressive gene expression, also in established hybrid lineages or species. Such extreme patterns of gene expression in stabilized hybrid taxa suggest that altered hybrid gene expression may result in hybridization‐derived evolutionary novelty. We also conclude that while patterns of misexpression in hybrids are well documented, the understanding of the mechanisms causing misexpression is lagging. We argue that jointly assessing differences in cell composition and cell‐specific changes in gene expression in hybrids, in addition to assessing changes in chromatin and methylation, will significantly advance our understanding of the basis of altered gene expression. Moreover, uncovering to what extent evolution of gene expression results in altered expression for individual genes, or entire networks of genes, will advance our understanding of how selection moulds gene expression. Finally, we argue that jointly studying the dual roles of altered hybrid gene expression, serving both as a mechanism for reproductive isolation and as a substrate for hybrid ecological adaptation, will lead to significant advances in our understanding of the evolution of gene expression.

Remote automated surveillance of insect abundance and diversity is poised to revolutionize insect decline studies. The study reveals spectral analysis of thin‐film wing interference signals (WISs) can discriminate free‐flying insects beyond what can be accomplished by machine vision. Detectable by photonic sensors, WISs are robust indicators enabling species and sex identification. The first quantitative survey of insect wing thickness and modulation through shortwave‐infrared hyperspectral imaging of 600 wings from 30 hover fly species is presented. Fringy spectral reflectance of WIS can be explained by four optical parameters, including membrane thickness. Using a Naïve Bayes Classifier with five parameters that can be retrieved remotely, 91% is achieved accuracy in identification of species and sexes. WIS‐based surveillance is therefore a potent tool for remote insect identification and surveillance.

Adaptation to novel ecological niches is known to be rapid. However, how the loci underlying ecological divergence are coupled to traits reproductively isolating populations, ultimately enabling the formation of persistent species, remains a consequential question in speciation research. Here, we investigated the genomic differences underpinning colonization of a new niche and formation of two partly sympatric host races of Tephritis conura peacock flies. We took advantage of two independent sympatric zones west and east of the Baltic Sea, where host plant specialists using the thistle species Cirsium heterophyllum and C. oleraceum co-occur, and address what regions of the genome maintain the host races in parallel. Using genome-wide association, differentiation and divergence statistics, we identified a large, highly divergent region associated with host use among western and eastern populations. Within this region, we identified unique haplotypes associated with each host race, indicative of a large inversion, adding to the growing body of evidence that structural changes to the genome are important for adaptations to persist in the face of gene flow. We further showed strong signatures of selection in this region, especially in populations of the derived C. oleraceum specialist host race. The region also had reduced introgression, especially in western populations, while the rest of the genome showed signs of extensive gene flow. Genes within highly differentiated windows within the putative inversion were not only enriched for functions involved in host adaptation, including phenology and metabolic responses to different metabolites in the two host plants, but also enriched for gametogenesis, fertilization and embryological development, all of which suggest sequence divergence could have large consequences on reproductive isolation between the host races. In conclusion, this study suggests that structural changes in the genome may facilitate the formation of persistent host races, and ultimately speciation, in face of gene flow.

Due to the growing awareness that insects' diversity and populations are in decline, there is an increased need for monitoring insects. Entomological lidars and photonic sensors can monitor and remotely identify flying insects based on their backscattered signal in terms of oscillations-, polarization-, and spectral content. The backscattered light from insects is predominantly oscillatory and derives from the wings. This part of the signal is also more coherent and co-polarized than the light reflected from the insect's abdomen. Clear membranes can display soap-bubble colors due to thin-film interference, a feature that can be associated with the thickness of the wing. A hyperspectral camera can capture these wing interference patterns with hundreds of spectral bands and accurately identify the wing thickness. Here we investigate whether the spectral fringes can provide complementary information to aid remote species identification. We demonstrate that we can extract wing thickness and modulation depth information from spectral fringes of 87 species of common insect pollinators in Skåne, Sweden. The modulation depth of a fringe provides information related to insect wing thickness homogeneity, wrinkledness, or anti-reflectance features. Our results show that examined species display distinct modulation and wing thickness, and therefore such features can be used to improve the specificity of species identification of photonics sensors.