Digest: Asymmetrical introgression of belly coloration across a manakin hybrid zone in Panama.

How does sexual selection impact introgression dynamics across a hybrid zone? Long et al. (2024) used historical (1989-1994) and contemporary (2017-2020) samples to quantify the stability of a Panamanian hybrid zone between golden-collared manakin birds (Manacus vitellinus) and white-collared manakins (M. candei). Their analyses revealed a spatially stable hybrid zone, except for one trait, belly plumage coloration, which has introgressed into the distribution of the white-collared manakin. This finding suggests possible sexual selection for this trait.

Digest: Understanding the evolution of sexual dichromatism also requires a female perspective.

The study of sexual dichromatism has generally focused on sexual selection for conspicuous males, ignoring the potential role played by selection in females. To address this problem, Price et al. took into account evolutionary changes in both males and females when investigating the evolution of plumage dichromatism across the New World blackbirds (Icteridae). They found that sexual dichromatism was repeatedly and rapidly lost as females evolved male-like plumage traits. The evolutionary dynamics in plumage coloration were drastically different in males and females, highlighting the importance of considering both perspectives in trait evolution.

Digest: Massive mixing and merging of Madagascar Gemsnakes.

Introgressive hybridization can give rise to reticulated patterns in a phylogeny. In a recent study, DeBaun et al. detected 12 reticulation events across the phylogeny of the Madagascar Gemsnakes, suggesting that their evolutionary history cannot be captured in a bifurcating tree. Moreover, identifying the true network of a group is difficult when using only available extant data. The evolution of these snakes might thus be even more tangled than we currently think.

Highly differentiated loci resolve phylogenetic relationships in the Bean Goose complex.

BACKGROUND: Reconstructing phylogenetic relationships with genomic data remains a challenging endeavor. Numerous phylogenomic studies have reported incongruent gene trees when analyzing different genomic regions, complicating the search for a 'true' species tree. Some authors have argued that genomic regions of increased divergence (i.e. differentiation islands) reflect the species tree, although other studies have shown that these regions might produce misleading topologies due to species-specific selective sweeps or ancient introgression events. In this study, we tested the extent to which highly differentiated loci can resolve phylogenetic relationships in the Bean Goose complex, a group of goose taxa that includes the Taiga Bean Goose (Anser fabalis), the Tundra Bean Goose (Anser serrirostris) and the Pink-footed Goose (Anser brachyrhynchus). RESULTS: First, we show that a random selection of genomic loci-which mainly samples the undifferentiated regions of the genome-results in an unresolved species complex with a monophyletic A. brachyrhynchus embedded within a paraphyletic cluster of A. fabalis and A. serrirostris. Next, phylogenetic analyses of differentiation islands converged upon a topology of three monophyletic clades in which A. brachyrhynchus is sister to A. fabalis, and A. serrirostris is sister to the clade uniting these two species. Close inspection of the locus trees within the differentiated regions revealed that this topology was consistently supported over other phylogenetic arrangements. As it seems unlikely that selection or introgression events have impacted all differentiation islands in the same way, we are convinced that this topology reflects the 'true' species tree. Additional analyses, based on D-statistics, revealed extensive introgression between A. fabalis and A. serrirostris, which partly explains the failure to resolve the species complex with a random selection of genomic loci. Recent introgression between these taxa has probably erased the phylogenetic branching pattern across a large section of the genome, whereas differentiation islands were unaffected by the homogenizing gene flow and maintained the phylogenetic patterns that reflect the species tree. CONCLUSIONS: The evolution of the Bean Goose complex can be depicted as a simple bifurcating tree, but this would ignore the impact of introgressive hybridization. Hence, we advocate that the evolutionary relationships between these taxa are best represented as a phylogenetic network.

Digest: Exploring the interplay between migration and speciation in the barn swallow.

When members of the same population follow distinct migration routes, a migratory divide can arise. Could differences in migratory strategies contribute to genetic differentiation and possibly speciation? In this study, Turbek et al. combine genomic data, stable isotopes, and geolocators to characterize a migratory divide between two subspecies of the barn swallow (Hirundo rustica). Their findings set the stage for further analyses into the genetic basis of migratory behavior.

Comparative Genomics of the Waterfowl Innate Immune System.

Animal species differ considerably in their ability to fight off infections. Finding the genetic basis of these differences is not easy, as the immune response is comprised of a complex network of proteins that interact with one another to defend the body against infection. Here, we used population- and comparative genomics to study the evolutionary forces acting on the innate immune system in natural hosts of the avian influenza virus (AIV). For this purpose, we used a combination of hybrid capture, next- generation sequencing and published genomes to examine genetic diversity, divergence, and signatures of selection in 127 innate immune genes at a micro- and macroevolutionary time scale in 26 species of waterfowl. We show across multiple immune pathways (AIV-, toll-like-, and RIG-I -like receptors signalling pathways) that genes involved genes in pathogen detection (i.e., toll-like receptors) and direct pathogen inhibition (i.e., antimicrobial peptides and interferon-stimulated genes), as well as host proteins targeted by viral antagonist proteins (i.e., mitochondrial antiviral-signaling protein, [MAVS]) are more likely to be polymorphic, genetically divergent, and under positive selection than other innate immune genes. Our results demonstrate that selective forces vary across innate immune signaling signalling pathways in waterfowl, and we present candidate genes that may contribute to differences in susceptibility and resistance to infectious diseases in wild birds, and that may be manipulated by viruses. Our findings improve our understanding of the interplay between host genetics and pathogens, and offer the opportunity for new insights into pathogenesis and potential drug targets.

Digest: Recent movement of a flicker hybrid zone.

What biotic and abiotic factors drive hybrid zone movement? By resampling a classic hybrid zone between two subspecies of woodpeckers, Aguillon and Rohwer documented a westward shift that may be attributed to changes in land use or climate. These findings highlight the increasing influence of anthropogenic activities on hybridization events.

Digest: Great tits and their ticks: Life-history traits affect tick fitness.

Ectoparasites such as ticks face many challenges to reproduce. They must maximize the size of their blood meal while avoiding being removed by their host. In a new study, Fracasso and colleagues followed the fate of individual ticks to determine which life-history traits impact tick fitness. Their findings reveal a complex interplay between numerous parameters, including feeding time and engorgement weight. The situation is likely even more complicated when considering vector-borne pathogens.

Avian Introgression Patterns are Consistent With Haldane's Rule.

According to Haldane's Rule, the heterogametic sex will show the greatest fitness reduction in a hybrid cross. In birds, where sex is determined by a ZW system, female hybrids are expected to experience lower fitness compared to male hybrids. This pattern has indeed been observed in several bird groups, but it is unknown whether the generality of Haldane's Rule also extends to the molecular level. First, given the lower fitness of female hybrids, we can expect maternally inherited loci (i.e., mitochondrial and W-linked loci) to show lower introgression rates than biparentally inherited loci (i.e., autosomal loci) in females. Second, the faster evolution of Z-linked loci compared to autosomal loci and the hemizygosity of the Z-chromosome in females might speed up the accumulation of incompatible alleles on this sex chromosome, resulting in lower introgression rates for Z-linked loci than for autosomal loci. I tested these expectations by conducting a literature review which focused on studies that directly quantified introgression rates for autosomal, sex-linked, and mitochondrial loci. Although most studies reported introgression rates in line with Haldane's Rule, it remains important to validate these genetic patterns with estimates of hybrid fitness and supporting field observations to rule out alternative explanations. Genomic data provide exciting opportunities to obtain a more fine-grained picture of introgression rates across the genome, which can consequently be linked to ecological and behavioral observations, potentially leading to novel insights into the genetic mechanisms underpinning Haldane's Rule.

Digest: Following clines along an Amazonian hybrid zone.

The shape and position of clines can provide crucial insights into the evolutionary forces at work in hybrid zones. In this issue, Del-Rio and colleagues applied cline theory to a hybrid zone between two antbird species in Amazonia. A narrow and displaced mitochondrial cline suggests that the selected genetic marker failed to track the northward movement of this hybrid zone, possibly due to reduced fitness of female hybrids.

Sexually dichromatic hybrids between two monochromatic duck species, the Chiloé wigeon and the Philippine duck.

Captive bird hybrids can provide important data on certain traits, such as hybrid viability and fertility. In this paper, we describe four hybrids between the Chiloé wigeon (Anas sibilatrix) and the Philippine duck (Anas luzonica). These two species diverged about 13 million years ago and are found on different continents, making the occurrence of wild hybrids extremely unlikely. Hence, these captive hybrids provide a unique opportunity to learn more about the outcome of hybridization between these highly divergent species. One pair of hybrids mated and produced six unfertilized eggs, suggesting that hybrids between these species are infertile. Morphologically, the hybrids were slightly larger than the parental species, but had intermediate bill lengths. With regard to plumage patterns, the hybrids displayed characteristics of both parental species: Males developed the iridescent green head pattern of the Chiloé wigeon, whereas the females showed the dark crown and eye stripe of the Philippine duck. Interestingly, Chiloé wigeon and Philippine duck are both sexually monochromatic whereas the hybrids showed clear sexual dimorphism. These hybrids can thus lead to novel insights into the genetic and developmental basis of sexual mono- and dichromatism in ducks.

The genic view of hybridization in the Anthropocene.

Human impact is noticeable around the globe, indicating that a new era might have begun: the Anthropocene. Continuing human activities, including land-use changes, introduction of non-native species and rapid climate change, are altering the distributions of countless species, often giving rise to human-mediated hybridization events. While the interbreeding of different populations or species can have detrimental effects, such as genetic extinction, it can be beneficial in terms of adaptive introgression or an increase in genetic diversity. In this paper, I first review the different mechanisms and outcomes of anthropogenic hybridization based on literature from the last five years (2016-2020). The most common mechanisms leading to the interbreeding of previously isolated taxa include habitat change (51% of the studies) and introduction of non-native species (34% intentional and 19% unintentional). These human-induced hybridization events most often result in introgression (80%). The high incidence of genetic exchange between the hybridizing taxa indicates that the application of a genic view of speciation (and introgression) can provide crucial insights on how to address hybridization events in the Anthropocene. This perspective considers the genome as a dynamic collection of genetic loci with distinct evolutionary histories, giving rise to a heterogenous genomic landscape in terms of genetic differentiation and introgression. First, understanding this genomic landscape can lead to a better selection of diagnostic genetic markers to characterize hybrid populations. Second, describing how introgression patterns vary across the genome can help to predict the likelihood of negative processes, such as demographic and genetic swamping, as well as positive outcomes, such as adaptive introgression. It is especially important to not only quantify how much genetic material introgressed, but also what has been exchanged. Third, comparing introgression patterns in pre-Anthropocene hybridization events with current human-induced cases might provide novel insights into the likelihood of genetic swamping or species collapse during an anthropogenic hybridization event. However, this comparative approach remains to be tested before it can be applied in practice. Finally, the genic view of introgression can be combined with conservation genomic studies to determine the legal status of hybrids and take appropriate measures to manage anthropogenic hybridization events. The interplay between evolutionary and conservation genomics will result in the constant exchange of ideas between these fields which will not only improve our knowledge on the origin of species, but also how to conserve and protect them.

Digest: Population genomics reveals convergence toward melanism in different island populations.

Distinct traits between mainland and island populations provide an excellent opportunity to study the evolution and genetic basis of these traits. In this issue, Walsh et al. unraveled the evolution of black plumage color that arose independently in two island populations of the white-winged fairywren. They also described the first steps in understanding the genetic underpinnings of this trait.

Genome Size Reduction and Transposon Activity Impact tRNA Gene Diversity While Ensuring Translational Stability in Birds.

As a highly diverse vertebrate class, bird species have adapted to various ecological systems. How this phenotypic diversity can be explained genetically is intensively debated and is likely grounded in differences in the genome content. Larger and more complex genomes could allow for greater genetic regulation that results in more phenotypic variety. Surprisingly, avian genomes are much smaller compared to other vertebrates but contain as many protein-coding genes as other vertebrates. This supports the notion that the phenotypic diversity is largely determined by selection on non-coding gene sequences. Transfer RNAs (tRNAs) represent a group of non-coding genes. However, the characteristics of tRNA genes across bird genomes have remained largely unexplored. Here, we exhaustively investigated the evolution and functional consequences of these crucial translational regulators within bird species and across vertebrates. Our dense sampling of 55 avian genomes representing each bird order revealed an average of 169 tRNA genes with at least 31% being actively used. Unlike other vertebrates, avian tRNA genes are reduced in number and complexity but are still in line with vertebrate wobble pairing strategies and mutation-driven codon usage. Our detailed phylogenetic analyses further uncovered that new tRNA genes can emerge through multiplication by transposable elements. Together, this study provides the first comprehensive avian and cross-vertebrate tRNA gene analyses and demonstrates that tRNA gene evolution is flexible albeit constrained within functional boundaries of general mechanisms in protein translation.

Digest: The interplay between imprinting, mimicry, and multimodal signaling can lead to sympatric speciation†.

Mimicry can directly affect the evolutionary history of models, mimics, and signal receivers. Mimics often use multimodal signaling to deceive receivers. Jamie et al. showed that brood parasitic birds display multimodal signaling of mimetic traits triggered by sexual and filial imprinting on host species. These resulting adaptations can interact with premating isolation barriers to strengthen reproductive isolation and potentially drive sympatric speciation.

Digest: Possible solutions for the joint estimation of divergence times and shared demographic changes.

Can we simultaneously infer divergence times and shared demographic events? Oaks et al. introduce a full-likelihood Bayesian method based on genomic data and show that this endeavor remains challenging. Their exercise also reveals some promising avenues for future modeling attempts.

Digest: How the snowshoe hare got its brown coat: Convergent evolution or gene flow?

The winter-brown phenotype of snowshoe hares in the Pacific Northwest was acquired through hybridization with black-tailed jackrabbits. Some snowshoe hares in more northern boreal populations exhibit the same phenotype, but how did they acquire it? Jones and colleagues show that the phenotype in the boreal populations is the outcome of convergent evolution, highlighting the importance of understanding the genetic basis of a trait in reconstructing its evolution.

How common is avian hybridization on an individual level?

Hybridization among different bird species is relatively common, but the hybridization rate of individuals is not well known. Justyn et al. use data from the citizen science project eBird to assess the individual hybridization rate in birds, showing that 0.064% of individuals are hybrids. The accuracy of this new estimate is affected by potential biases introduced by birdwatchers, such as over-reporting of rare hybrids and under-reporting of difficult-to-identify hybrids.

Digest: Climate change and agricultural intensification influence the strength and direction of natural selection in tree swallows.

How does environmental heterogeneity affect natural selection on tree swallow nestlings? Houle et al. (2020) show that more precipitation and higher temperatures result in stronger selection on body mass and wing length and that agricultural intensity can affect the direction of selection. These findings raise the question of how genetic diversity changes under strong selection pressures, which will be especially important under ongoing agriculture intensification and climate change.

Recent introgression between Taiga Bean Goose and Tundra Bean Goose results in a largely homogeneous landscape of genetic differentiation.

Several studies have uncovered a highly heterogeneous landscape of genetic differentiation across the genomes of closely related species. Specifically, genetic differentiation is often concentrated in particular genomic regions ("islands of differentiation") that might contain barrier loci contributing to reproductive isolation, whereas the rest of the genome is homogenized by introgression. Alternatively, linked selection can produce differentiation islands in allopatry without introgression. We explored the influence of introgression on the landscape of genetic differentiation in two hybridizing goose taxa: the Taiga Bean Goose (Anser fabalis) and the Tundra Bean Goose (A. serrirostris). We re-sequenced the whole genomes of 18 individuals (9 of each taxon) and, using a combination of population genomic summary statistics and demographic modeling, we reconstructed the evolutionary history of these birds. Next, we quantified the impact of introgression on the build-up and maintenance of genetic differentiation. We found evidence for a scenario of allopatric divergence (about 2.5 million years ago) followed by recent secondary contact (about 60,000 years ago). Subsequent introgression events led to high levels of gene flow, mainly from the Tundra Bean Goose into the Taiga Bean Goose. This scenario resulted in a largely undifferentiated genomic landscape (genome-wide FST = 0.033) with a few notable differentiation peaks that were scattered across chromosomes. The summary statistics indicated that some peaks might contain barrier loci while others arose in allopatry through linked selection. Finally, based on the low genetic differentiation, considerable morphological variation and incomplete reproductive isolation, we argue that the Taiga and the Tundra Bean Goose should be treated as subspecies.