The Role of Hybridization in Species Formation and Persistence.

Hybridization, or interbreeding between different taxa, was traditionally considered to be rare and to have a largely detrimental impact on biodiversity, sometimes leading to the breakdown of reproductive isolation and even to the reversal of speciation. However, modern genomic and analytical methods have shown that hybridization is common in some of the most diverse clades across the tree of life, sometimes leading to rapid increase of phenotypic variability, to introgression of adaptive alleles, to the formation of hybrid species, and even to entire species radiations. In this review, we identify consensus among diverse research programs to show how the field has progressed. Hybridization is a multifaceted evolutionary process that can strongly influence species formation and facilitate adaptation and persistence of species in a rapidly changing world. Progress on testing this hypothesis will require cooperation among different subdisciplines.

Hybridization and gene expression: Beyond differentially expressed genes.

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.

Evolutionary plant-pollinator responses to anthropogenic land-use change: impacts on ecosystem services.

Agricultural intensification at field and landscape scales, including increased use of agrochemicals and loss of semi-natural habitats, is a major driver of insect declines and other community changes. Efforts to understand and mitigate these effects have traditionally focused on ecological responses. At the same time, adaptations to pesticide use and habitat fragmentation in both insects and flowering plants show the potential for rapid evolution. Yet we lack an understanding of how such evolutionary responses may propagate within and between trophic levels with ensuing consequences for conservation of species and ecological functions in agroecosystems. Here, we review the literature on the consequences of agricultural intensification on plant and animal evolutionary responses and interactions. We present a novel conceptualization of evolutionary change induced by agricultural intensification at field and landscape scales and emphasize direct and indirect effects of rapid evolution on ecosystem services. We exemplify by focusing on economically and ecologically important interactions between plants and pollinators. We showcase available eco-evolutionary theory and plant-pollinator modelling that can improve predictions of how agricultural intensification affects interaction networks, and highlight available genetic and trait-focused methodological approaches. Specifically, we focus on how spatial genetic structure affects the probability of propagated responses, and how the structure of interaction networks modulates effects of evolutionary change in individual species. Thereby, we highlight how combined trait-based eco-evolutionary modelling, functionally explicit quantitative genetics, and genomic analyses may shed light on conditions where evolutionary responses impact important ecosystem services.

Discrimination of Hover Fly Species and Sexes by Wing Interference Signals.

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.

Remote Nanoscopy with Infrared Elastic Hyperspectral Lidar.

Monitoring insects of different species to understand the factors affecting their diversity and decline is a major challenge. Laser remote sensing and spectroscopy offer promising novel solutions to this. Coherent scattering from thin wing membranes also known as wing interference patterns (WIPs) have recently been demonstrated to be species specific. The colors of WIPs arise due to unique fringy spectra, which can be retrieved over long distances. To demonstrate this, a new concept of infrared (950-1650 nm) hyperspectral lidar with 64 spectral bands based on a supercontinuum light source using ray-tracing and 3D printing is developed. A lidar with an unprecedented number of spectral channels, high signal-to-noise ratio, and spatio-temporal resolution enabling detection of free-flying insects and their wingbeats. As proof of principle, coherent scatter from a damselfly wing at 87 m distance without averaging (4 ms recording) is retrieved. The fringed signal properties are used to determine an effective wing membrane thickness of 1412 nm with ±4 nm precision matching laboratory recordings of the same wing. Similar signals from free flying insects (2 ms recording) are later recorded. The accuracy and the method's potential are discussed to discriminate species by capturing coherent features from free-flying insects.

A biophotonic platform for quantitative analysis in the spatial, spectral, polarimetric, and goniometric domains.

Advanced instrumentation and versatile setups are needed for understanding light interaction with biological targets. Such instruments include (1) microscopes and 3D scanners for detailed spatial analysis, (2) spectral instruments for deducing molecular composition, (3) polarimeters for assessing structural properties, and (4) goniometers probing the scattering phase function of, e.g., tissue slabs. While a large selection of commercial biophotonic instruments and laboratory equipment are available, they are often bulky and expensive. Therefore, they remain inaccessible for secondary education, hobbyists, and research groups in low-income countries. This lack of equipment impedes hands-on proficiency with basic biophotonic principles and the ability to solve local problems with applied physics. We have designed, prototyped, and evaluated the low-cost Biophotonics, Imaging, Optical, Spectral, Polarimetric, Angular, and Compact Equipment (BIOSPACE) for high-quality quantitative analysis. BIOSPACE uses multiplexed light-emitting diodes with emission wavelengths from ultraviolet to near-infrared, captured by a synchronized camera. The angles of the light source, the target, and the polarization filters are automated by low-cost mechanics and a microcomputer. This enables multi-dimensional scatter analysis of centimeter-sized biological targets. We present the construction, calibration, and evaluation of BIOSPACE. The diverse functions of BIOSPACE include small animal spectral imaging, measuring the nanometer thickness of a bark-beetle wing, acquiring the scattering phase function of a blood smear and estimating the anisotropic scattering and the extinction coefficients, and contrasting muscle fibers using polarization. We provide blueprints, component list, and software for replication by enthusiasts and educators to simplify the hands-on investigation of fundamental optical properties in biological samples.

Weak population genetic structure in Eurasian spruce bark beetle over large regional scales in Sweden.

The Eurasian spruce bark beetle, Ips typographus, is a major pest, capable of killing spruce forests during large population outbreaks. Recorded dispersal distances of individual beetles are typically within hundreds of meters or a few kilometers. However, the connectivity between populations at larger distances and longer time spans and how this is affected by the habitat is less studied, despite its importance for understanding at which distances local outbreaks may spread. Previous population genetic studies in I. typographus typically used low resolution markers. Here, we use genome-wide data to assess population structure and connectivity of I. typographus in Sweden. We used 152 individuals from 19 population samples, distributed over 830 km from Strömsund (63° 46' 8″ N) in the north to Nyteboda (56° 8' 50″ N) in the south, to capture processes at a large regional scale, and a transect sampling design adjacent to a recent outbreak to capture processes at a smaller scale (76 km). Using restriction site-associated DNA sequencing (RADseq) markers capturing 1409-1997 SNPs throughout the genome, we document a weak genetic structure over the large scale, potentially indicative of high connectivity with extensive gene flow. No differentiation was detected at the smaller scale. We find indications of isolation-by-distance both for relative (F ST) and absolute divergence (Dxy). The two northernmost populations are most differentiated from the remaining populations, and diverge in parallel to the southern populations for a set of outlier loci. In conclusion, the population structure of I. typographus in Sweden is weak, suggesting a high capacity to disperse and establish outbreak populations in new territories.

Extensive transgressive gene expression in testis but not ovary in the homoploid hybrid Italian sparrow.

Hybridization can result in novel allelic combinations which can impact the hybrid phenotype through changes in gene expression. While misexpression in F1 hybrids is well documented, how gene expression evolves in stabilized hybrid taxa remains an open question. As gene expression evolves in a stabilizing manner, break-up of co-evolved cis- and trans-regulatory elements could lead to transgressive patterns of gene expression in hybrids. Here, we address to what extent gonad gene expression has evolved in an established and stable homoploid hybrid, the Italian sparrow (Passer italiae). Through comparison of gene expression in gonads from individuals of the two parental species (i.e., house and Spanish sparrow) to that of Italian sparrows, we find evidence for strongly transgressive expression in male Italian sparrows-2530 genes (22% of testis genes tested for inheritance) exhibit expression patterns outside the range of both parent species. In contrast, Italian sparrow ovary expression was similar to that of one of the parent species, the house sparrow (Passer domesticus). Moreover, the Italian sparrow testis transcriptome is 26 times as diverged from those of the parent species as the parental transcriptomes are from each other, despite being genetically intermediate. This highlights the potential for regulation of gene expression to produce novel variation following hybridization. Genes involved in mitochondrial respiratory chain complexes and protein synthesis are enriched in the subset that is over-dominantly expressed in Italian sparrow testis, suggesting that selection on key functions has moulded the hybrid Italian sparrow transcriptome.

Predictors of genomic differentiation within a hybrid taxon.

Hybridization is increasingly recognized as an important evolutionary force. Novel genetic methods now enable us to address how the genomes of parental species are combined in hybrid lineages. However, we still do not know the relative importance of admixed proportions, genome architecture and local selection in shaping hybrid genomes. Here, we take advantage of the genetically divergent island populations of Italian sparrow on Crete, Corsica and Sicily to investigate the predictors of genomic variation within a hybrid taxon. We test if differentiation is affected by recombination rate, selection, or variation in ancestry proportions. We find that the relationship between recombination rate and differentiation is less pronounced within hybrid lineages than between the parent species, as expected if purging of minor parent ancestry in low recombination regions reduces the variation available for differentiation. In addition, we find that differentiation between islands is correlated with differences in signatures of selection in two out of three comparisons. Signatures of selection within islands are correlated across all islands, suggesting that shared selection may mould genomic differentiation. The best predictor of strong differentiation within islands is the degree of differentiation from house sparrow, and hence loci with Spanish sparrow ancestry may vary more freely. Jointly, this suggests that constraints and selection interact in shaping the genomic landscape of differentiation in this hybrid species.

Correlational selection in the age of genomics.

Ecologists and evolutionary biologists are well aware that natural and sexual selection do not operate on traits in isolation, but instead act on combinations of traits. This long-recognized and pervasive phenomenon is known as multivariate selection, or-in the particular case where it favours correlations between interacting traits-correlational selection. Despite broad acknowledgement of correlational selection, the relevant theory has often been overlooked in genomic research. Here, we discuss theory and empirical findings from ecological, quantitative genetic and genomic research, linking key insights from different fields. Correlational selection can operate on both discrete trait combinations and quantitative characters, with profound implications for genomic architecture, linkage, pleiotropy, evolvability, modularity, phenotypic integration and phenotypic plasticity. We synthesize current knowledge and discuss promising research approaches that will enable us to understand how correlational selection shapes genomic architecture, thereby linking quantitative genetic approaches with emerging genomic methods. We suggest that research on correlational selection has great potential to integrate multiple fields in evolutionary biology, including developmental and functional biology, ecology, quantitative genetics, phenotypic polymorphisms, hybrid zones and speciation processes.

Bark beetles as lidar targets and prospects of photonic surveillance.

Forestry is raising concern about the outbreaks of European spruce bark beetle, Ips typographus, causing extensive damage to the spruce forest and timber values. Precise monitoring of these beetles is a necessary step towards preventing outbreaks. Current commercial monitoring methods are catch-based and lack in both temporal and spatial resolution. In this work, light scattering from beetles is characterized, and the feasibility of entomological lidar as a tool for long-term monitoring of bark beetles is explored. Laboratory optical properties, wing thickness, and wingbeat frequency of bark beetles are reported, and these parameters can infer target identity in lidar data. Lidar results from a Swedish forest with controlled bark beetle release event are presented. The capability of lidar to simultaneously monitor both insects and a pheromone plume mixed with chemical smoke governing the dispersal of many insects is demonstrated. In conclusion, entomological lidar is a promising tool for monitoring bark beetles.

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics.

Sexually antagonistic (SA) genetic variation-in which alleles favored in one sex are disfavored in the other-is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterization of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research-including F ST and F IS statistics, genome-wide association studies, pedigree analyses, reciprocal transplant studies, and evolve-and-resequence experiments-to evaluate methods for identifying SA genes and genome-wide signals of SA genetic variation. We begin by developing theoretical models for between-sex F ST and F IS, including explicit null distributions for each statistic, and using them to critically evaluate putative multilocus signals of sex-specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of F ST and F IS, along with applications of more direct approaches for characterizing SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work.

Eukaryote hybrid genomes.

Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adaptation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve.

Hybridization, sex-specific genomic architecture and local adaptation.

While gene flow can reduce the potential for local adaptation, hybridization may conversely provide genetic variation that increases the potential for local adaptation. Hybridization may also affect adaptation through altering sexual dimorphism and sexual conflict, but this remains largely unstudied. Here, we discuss how hybridization may affect sexual dimorphism and conflict due to differential effects of hybridization on males and females, and then how this, in turn, may affect local adaptation. First, in species with heterochromatic sexes, the lower viability of the heterogametic sex in hybrids could shift the balance in sexual conflict. Second, sex-specific inheritance of the mitochondrial genome in hybrids may lead to cytonuclear mismatches, for example, in the form of 'mother's curse', with potential consequences for sex ratio and sex-specific expression. Third, sex-biased introgression and recombination may lead to sex-specific consequences of hybridization. Fourth, transgressive segregation of sexually antagonistic alleles could increase sexual dimorphism in hybrid populations. Sexual dimorphism can reduce sexual conflict and enhance intersexual niche partitioning, increasing the fitness of hybrids. Adaptive introgression of alleles reducing sexual conflict or enhancing intersexual niche partitioning may facilitate local adaptation, and could favour the colonization of novel habitats. We review these consequences of hybridization on sex differences and local adaptation, and discuss how their prevalence and importance could be tested empirically.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Can the narrow red bands of dragonflies be used to perceive wing interference patterns?

Despite numerous studies of selection on position and number of spectral vision bands, explanations to the function of narrow spectral bands are lacking. We investigate dragonflies (Odonata), which have the narrowest spectral bands reported, in order to investigate what features these narrow spectral bands may be used to perceive. We address whether it is likely that narrow red bands can be used to identify conspecifics by the optical signature from wing interference patterns (WIPs). We investigate the optical signatures of Odonata wings using hyperspectral imaging, laser profiling, ellipsometry, polarimetric modulation spectroscopy, and laser radar experiments. Based on results, we estimate the prospects for Odonata perception of WIPs to identify conspecifics in the spectral, spatial, intensity, polarization, angular, and temporal domains. We find six lines of evidence consistent with an ability to perceive WIPs. First, the wing membrane thickness of the studied Odonata is 2.3 µm, coinciding with the maximal thickness perceivable by the reported bandwidth. Second, flat wings imply that WIPs persist from whole wings, which can be seen at a distance. Third, WIPs constitute a major brightness in the visual environment only second after the solar disk. Fourth, WIPs exhibit high degree of polarization and polarization vision coincides with frontal narrow red bands in Odonata. Fifth, the angular light incidence on the Odonata composite eye provides all prerequisites for direct assessment of the refractive index which is associated with age. Sixth, WIPs from conspecifics in flight make a significant contribution even to the fundamental wingbeat frequency within the flicker fusion bandwidth of Odonata vision. We conclude that it is likely that WIPs can be perceived by the narrow red bands found in some Odonata species and propose future behavioral and electrophysiological tests of this hypothesis.

Genomic Contingencies and the Potential for Local Adaptation in a Hybrid Species.

Hybridization is increasingly recognized as a potent evolutionary force. Although additive genetic variation and novel combinations of parental genes theoretically increase the potential for hybrid species to adapt, few empirical studies have investigated the adaptive potential within a hybrid species. Here, we address whether genomic contingencies, adaptation to climate, or diet best explain divergence in beak morphology using genomically diverged island populations of the homoploid hybrid Italian sparrow Passer italiae from Crete, Corsica, and Sicily. Populations vary significantly in beak morphology both between and within islands of origin. Temperature seasonality best explains population divergence in beak size. Interestingly, beak shape along all significant dimensions of variation was best explained by annual precipitation, genomic composition, and their interaction, suggesting a role for contingencies. Moreover, beak shape similarity to a parent species correlates with proportion of the genome inherited from that species, consistent with the presence of contingencies. In conclusion, adaptation to local conditions and genomic contingencies arising from putatively independent hybridization events jointly explain beak morphology in the Italian sparrow. Hence, hybridization may induce contingencies and restrict evolution in certain directions dependent on the genetic background.

Variation and constraints in hybrid genome formation.

Hybridization is an important source of variation; it transfers adaptive genetic variation across species boundaries and generates new species. Yet, the limits to viable hybrid genome formation are poorly understood. Here we investigated to what extent hybrid genomes are free to evolve by sequencing the genomes of four island populations of the homoploid hybrid Italian sparrow Passer italiae. We report that a variety of novel and fully functional hybrid genomic combinations are likely to have arisen independently on Crete, Corsica, Sicily and Malta, with differentiation in candidate genes for beak shape and plumage colour. However, certain genomic regions are invariably inherited from the same parent species, limiting variation. These regions are over-represented on the Z chromosome and harbour candidate incompatibility loci, including DNA-repair and mitonuclear genes. These gene classes may contribute to the general reduction of introgression on sex chromosomes. This study demonstrates that hybrid genomes may vary, and identifies new candidate reproductive isolation genes.

Linking intra- and interspecific assortative mating: Consequences for asymmetric sexual isolation.

Assortative mating is of interest because of its role in speciation and the maintenance of species boundaries. However, we know little about how within-species assortment is related to interspecific sexual isolation. Most previous studies of assortative mating have focused on a single trait in males and females, rather than utilizing multivariate trait information. Here, we investigate how intraspecific assortative mating relates to sexual isolation in two sympatric and congeneric damselfly species (genus Calopteryx). We connect intraspecific assortment to interspecific sexual isolation by combining field observations, mate preference experiments, and enforced copulation experiments. Using canonical correlation analysis, we demonstrate multivariate intraspecific assortment for body size and body shape. Males of the smaller species mate more frequently with heterospecific females than males of the larger species, which showed less attraction to small heterospecific females. Field experiments suggest that sexual isolation asymmetry is caused by male preferences for large heterospecific females, rather than by mechanical isolation due to interspecific size differences or female preferences for large males. Male preferences for large females and male-male competition for high quality females can therefore counteract sexual isolation. This sexual isolation asymmetry indicates that sexual selection currently opposes a species boundary.

Ecological explanations to island gigantism: dietary niche divergence, predation, and size in an endemic lizard.

Although rapid evolution of body size on islands has long been known, the ecological mechanisms behind this island phenomenon remain poorly understood. Diet is an important selective pressure for morphological divergence. Here we investigate if selection for novel diets has contributed to the multiple independent cases of island gigantism in the Skyros wall lizard (Podarcis gaigeae) and if diet, predation, or both factors best explain island gigantism. We combined data on body size, shape, bite force, and realized and available diets to address this. Several lines of evidence suggest that diet has contributed to the island gigantism. The larger islet lizards have relatively wider heads and higher bite performance in relation to mainland lizards than would be expected from size differences alone. The proportions of consumed and available hard prey are higher on islets than mainland localities, and lizard body size is significantly correlated with the proportion of hard prey. Furthermore, the main axis of divergence in head shape is significantly correlated with dietary divergence. Finally, a model with only diet and one including diet and predation regime explain body size divergence equally well. Our results suggest that diet is an important ecological factor behind insular body size divergence, but could be consistent with an additional role for predation.

Sex differences in developmental plasticity and canalization shape population divergence in mate preferences.

Sexual selection of high-quality mates can conflict with species recognition if traits that govern intraspecific mate preferences also influence interspecific recognition. This conflict might be resolved by developmental plasticity and learned mate preferences, which could drive preference divergence in populations that differ in local species composition. We integrate field and laboratory experiments on two calopterygid damselfly species with population genetic data to investigate how sex differences in developmental plasticity affect population divergence in the face of gene flow. Whereas male species recognition is fixed at emergence, females instead learn to recognize heterospecifics. Females are therefore more plastic in their mate preferences than males. We suggest that this results from sex differences in the balance between sexual selection for high-quality mates and selection for species recognition. As a result of these sex differences, females develop more pronounced population divergence in their mate preferences compared with males. Local ecological community context and presence of heterospecifics in combination with sex differences in plasticity and canalization therefore shape population divergence in mate preferences. As ongoing environmental change and habitat fragmentation bring formerly allopatric species into secondary contact, developmental plasticity of mate preferences in either or both sexes might facilitate coexistence and prevent local species extinction.