Complexity of avian evolution revealed by family-level genomes.

Despite tremendous efforts in the past decades, relationships among main avian lineages remain heavily debated without a clear resolution. Discrepancies have been attributed to diversity of species sampled, phylogenetic method and the choice of genomic regions1-3. Here we address these issues by analysing the genomes of 363 bird species4 (218 taxonomic families, 92% of total). Using intergenic regions and coalescent methods, we present a well-supported tree but also a marked degree of discordance. The tree confirms that Neoaves experienced rapid radiation at or near the Cretaceous-Palaeogene boundary. Sufficient loci rather than extensive taxon sampling were more effective in resolving difficult nodes. Remaining recalcitrant nodes involve species that are a challenge to model due to either extreme DNA composition, variable substitution rates, incomplete lineage sorting or complex evolutionary events such as ancient hybridization. Assessment of the effects of different genomic partitions showed high heterogeneity across the genome. We discovered sharp increases in effective population size, substitution rates and relative brain size following the Cretaceous-Palaeogene extinction event, supporting the hypothesis that emerging ecological opportunities catalysed the diversification of modern birds. The resulting phylogenetic estimate offers fresh insights into the rapid radiation of modern birds and provides a taxon-rich backbone tree for future comparative studies.

The evolution of sex roles: The importance of ecology and social environment.

Males and females often have different roles in reproduction, although the origin of these differences has remained controversial. Explaining the enigmatic reversed sex roles where males sacrifice their mating potential and provide full parental care is a particularly long-standing challenge in evolutionary biology. While most studies focused on ecological factors as the drivers of sex roles, recent research highlights the significance of social factors such as the adult sex ratio. To disentangle these propositions, here, we investigate the additive and interactive effects of several ecological and social factors on sex role variation using shorebirds (sandpipers, plovers, and allies) as model organisms that provide the full spectrum of sex role variation including some of the best-known examples of sex-role reversal. Our results consistently show that social factors play a prominent role in driving sex roles. Importantly, we show that reversed sex roles are associated with both male-skewed adult sex ratios and high breeding densities. Furthermore, phylogenetic path analyses provide general support for sex ratios driving sex role variations rather than being a consequence of sex roles. Together, these important results open future research directions by showing that different mating opportunities of males and females play a major role in generating the evolutionary diversity of sex roles, mating system, and parental care.

Divergent Selection in Low Recombination Regions Shapes the Genomic Islands in Two Incipient Shorebird Species.

Speciation in the face of gene flow is usually associated with a heterogeneous genomic landscape of divergence in nascent species pairs. However, multiple factors, such as divergent selection and local recombination rate variation, can influence the formation of these genomic islands. Examination of the genomic landscapes of species pairs that are still in the early stages of speciation provides an insight into this conundrum. In this study, population genomic analyses were undertaken using a wide range of sampling and whole-genome resequencing data from 96 unrelated individuals of Kentish plover (Charadrius alexandrinus) and white-faced plover (Charadrius dealbatus). We suggest that the two species exhibit varying levels of population admixture along the Chinese coast and on the Taiwan Island. Genome-wide analyses for introgression indicate that ancient introgression had occurred in Taiwan population, and gene flow is still ongoing in mainland coastal populations. Furthermore, we identified a few genomic regions with significant levels of interspecific differentiation and local recombination suppression, which contain several genes potentially associated with disease resistance, coloration, and regulation of plumage molting and thus may be relevant to the phenotypic and ecological divergence of the two nascent species. Overall, our findings suggest that divergent selection in low recombination regions may be a main force in shaping the genomic islands in two incipient shorebird species.

Role-reversed polyandry is associated with faster fast-Z in shorebirds.

In birds, males are homogametic and carry two copies of the Z chromosome ('ZZ'), while females are heterogametic and exhibit a 'ZW' genotype. The Z chromosome evolves at a faster rate than similarly sized autosomes, a phenomenon termed 'fast-Z evolution'. This is thought to be caused by two independent processes-greater Z chromosome genetic drift owing to a reduced effective population size, and stronger Z chromosome positive selection owing to the exposure of partially recessive alleles to selection. Here, we investigate the relative contributions of these processes by considering the effect of role-reversed polyandry on fast-Z in shorebirds, a paraphyletic group of wading birds that exhibit unusually diverse mating systems. We find stronger fast-Z effects under role-reversed polyandry, which is consistent with particularly strong selection on polyandrous females driving the fixation of recessive beneficial alleles. This result contrasts with previous research in birds, which has tended to implicate a primary role of genetic drift in driving fast-Z variation. We suggest that this discrepancy can be interpreted in two ways-stronger sexual selection acting on polyandrous females overwhelms an otherwise central role of genetic drift, and/or sexual antagonism is also contributing significantly to fast-Z and is exacerbated in sexually dimorphic species.

Successful conservation of global waterbird populations depends on effective governance.

Understanding global patterns of biodiversity change is crucial for conservation research, policies and practices. However, for most ecosystems, the lack of systematically collected data at a global level limits our understanding of biodiversity changes and their local-scale drivers. Here we address this challenge by focusing on wetlands, which are among the most biodiverse and productive of any environments and which provide essential ecosystem services, but are also amongst the most seriously threatened ecosystems. Using birds as an indicator taxon of wetland biodiversity, we model time-series abundance data for 461 waterbird species at 25,769 survey sites across the globe. We show that the strongest predictor of changes in waterbird abundance, and of conservation efforts having beneficial effects, is the effective governance of a country. In areas in which governance is on average less effective, such as western and central Asia, sub-Saharan Africa and South America, waterbird declines are particularly pronounced; a higher protected area coverage of wetland environments facilitates waterbird increases, but only in countries with more effective governance. Our findings highlight that sociopolitical instability can lead to biodiversity loss and undermine the benefit of existing conservation efforts, such as the expansion of protected area coverage. Furthermore, data deficiencies in areas with less effective governance could lead to underestimations of the extent of the current biodiversity crisis.

Myelofibrosis progression grading based on type I and type III collagen and fibrillin 1 expression boosted by whole slide image analysis.

AIMS: The progression of primary myelofibrosis is characterised by ongoing extracellular matrix deposition graded based on 'reticulin' and 'collagen' fibrosis, as revealed by Gomori's silver impregnation. Here we studied the expression of the major extracellular matrix proteins of fibrosis in relation to diagnostic silver grading supported by image analysis. METHODS AND RESULTS: By using automated immunohistochemistry, in this study we demonstrate that the expression of both types I and III collagens and fibrillin 1 by bone marrow stromal cells can reveal the extracellular matrix scaffolding in line with myelofibrosis progression as classified by silver grading. 'Reticulin' fibrosis indicated by type III collagen expression and 'collagen' fibrosis featured by type I collagen expression were parallel, rather than sequential, events. This is line with the proposed role of type III collagen in regulating type I collagen fibrillogenesis. The uniformly strong fibrillin 1 immune signals offered the best inter-rater agreements and the highest statistical correlations with silver grading of the three markers, which was robustly confirmed by automated whole slide digital image analysis using a machine learning-based algorithm. The progressive up-regulation of fibrillin 1 during myelofibrosis may result from a negative feedback loop as fibrillin microfibrils sequester TGF-ß, the major promoter of fibrosis. This can also reduce TGF-ß-induced RANKL levels, which would stimulate osteoclastogenesis and thus can support osteosclerosis in advanced myelofibrosis. CONCLUSIONS: Through the in-situ detection of these extracellular matrix proteins, our results verify the molecular pathobiology of fibrosis during myelofibrosis progression. In particular, fibrillin 1 immunohistochemistry, with or without image analysis, can complement diagnostic silver grading at decent cell morphology.

Evolution of reproductive modes in sharks and rays.

The ecological and life history drivers of the diversification of reproductive modes in early vertebrates are not fully understood. Sharks, rays and chimaeras (group Chondrichthyes) have an unusually diverse variety of reproductive modes and are thus an ideal group to test the factors driving the evolution of reproductive complexity. Here, using 960 species representing all major Chondrichthyes taxa, we reconstruct the evolution of their reproduction modes and investigate the ecological and life history predictors of reproduction. We show that the ancestral Chondrichthyes state was egg-laying and find multiple independent transitions between egg-laying and live-bearing via an intermediate state of yolk-only live-bearing. Using phylogenetically informed analysis, we also show that live-bearing species have larger body size and larger offspring than egg-laying species. In addition, live-bearing species are distributed over shallow to intermediate depths, while egg-layers are typically found in deeper waters. This suggests that live-bearing is more closely associated with pelagic, rather than demersal habitats. Taken together, using a basal vertebrate group as a model, we demonstrat how reproductive mode co-evolves with environmental conditions and life-history traits.

Multiple paternity is related to adult sex ratio and sex determination system in reptiles.

The adult sex ratio (ASR, the proportion of males in the adult population) is an emerging predictor of reproductive behaviour, and recent studies in birds and humans suggest it is a major driver of social mating systems and parental care. ASR may also influence genetic mating systems. For instance male-skewed ASRs are expected to increase the frequency of multiple paternity (defined here as a clutch or litter sired by two or more males) due to higher rates of coercive copulations by males, and/or due to females exploiting the opportunity of copulation with multiple males to increase genetic diversity of their offspring. Here, we evaluate this hypothesis in reptiles that often exhibit high frequency of multiple paternity although its ecological and life-history predictors have remained controversial. Using a comprehensive dataset of 81 species representing all four non-avian reptile orders, we show that increased frequency of multiple paternity is predicted by more male-skewed ASR, and this relationship is robust to simultaneous effects of several life-history predictors. Additionally, we show that the frequency of multiple paternity varies with the sex determination system: species with female heterogamety (ZZ/ZW sex chromosomes) exhibit higher levels of multiple paternity than species with male heterogamety (XY/XX) or temperature-dependent sex determination. Thus, our across-species comparative study provides the first evidence that genetic mating system depends on ASR in reptiles. We call for further investigations to uncover the complex evolutionary associations between mating systems, sex determination systems and ASR.

Sex differences in adult lifespan and aging rates of mortality across wild mammals.

In human populations, women consistently outlive men, which suggests profound biological foundations for sex differences in survival. Quantifying whether such sex differences are also pervasive in wild mammals is a crucial challenge in both evolutionary biology and biogerontology. Here, we compile demographic data from 134 mammal populations, encompassing 101 species, to show that the female's median lifespan is on average 18.6% longer than that of conspecific males, whereas in humans the female advantage is on average 7.8%. On the contrary, we do not find any consistent sex differences in aging rates. In addition, sex differences in median adult lifespan and aging rates are both highly variable across species. Our analyses suggest that the magnitude of sex differences in mammalian mortality patterns is likely shaped by local environmental conditions in interaction with the sex-specific costs of sexual selection.

Sex roles in birds: Phylogenetic analyses of the influence of climate, life histories and social environment.

Sex roles describe sex differences in courtship, mate competition, social pair-bonds and parental care. A key challenge is to identify associations among the components and the drivers of sex roles. Here, we investigate sex roles using data from over 1800 bird species. We found extensive variation and lability in proxies of sex roles, indicating remarkably independent evolution among sex role components. Climate and life history showed weak associations with sex roles. However, adult sex ratio is associated with sexual dimorphism, mating system and parental care, suggesting that social environment is central to explaining variation in sex roles among birds. Our results suggest that sex differences in reproductive behaviour are the result of diverse and idiosyncratic responses to selection. Further understanding of sex roles requires studies at the population level to test how local responses to ecology, life histories and mating opportunities drive processes that shape sex role variation among higher taxa.

Evolution of Social Organization: Phylogenetic Analyses of Ecology and Sexual Selection in Weavers.

AbstractCrook published a landmark study on the social organization of weavers (or weaverbirds, family Ploceidae) that contributed to the emergence of sociobiology, behavioral ecology, and phylogenetic comparative methods. By comparing ecology, spatial distribution, and mating systems, Crook suggested that the spatial distribution of food resources and breeding habitats influence weaver aggregation during both the nonbreeding season (flocking vs. solitary foraging) and the breeding season (colonial vs. solitary breeding), and the latter in turn impacts mating systems and sexual selection. Although Crook's study stimulated much follow-up research, his conclusions have not been scrutinized using phylogenetically controlled analyses. We revisited Crook's hypotheses using modern phylogenetic comparative methods on an extended data set of 107 weaver species. We showed that both diet and habitat type are associated with spatial distribution and that the latter predicts mating system, consistent with Crook's propositions. The best-supported phylogenetic path model also supported Crook's arguments and uncovered a direct relationship between nonbreeding distribution and mating system. Taken together, our phylogenetically corrected analyses confirm Crook's conjectures on the roles of ecology in social organizations of weavers; however, our analyses also uncovered an association between nonbreeding distributions and mating systems, which was not envisaged by Crook.

Sex differences in immune gene expression in the brain of a small shorebird.

Males and females often exhibit differences in behaviour, life histories, and ecology, many of which are typically reflected in their brains. Neuronal protection and maintenance include complex processes led by the microglia, which also interacts with metabolites such as hormones or immune components. Despite increasing interest in sex-specific brain function in laboratory animals, the significance of sex-specific immune activation in the brain of wild animals along with the variables that could affect it is widely lacking. Here, we use the Kentish plover (Charadrius alexandrinus) to study sex differences in expression of immune genes in the brain of adult males and females, in two wild populations breeding in contrasting habitats: a coastal sea-level population and a high-altitude inland population in China. Our analysis yielded 379 genes associated with immune function. We show a significant male-biased immune gene upregulation. Immune gene expression in the brain did not differ in upregulation between the coastal and inland populations. We discuss the role of dosage compensation in our findings and their evolutionary significance mediated by sex-specific survival and neuronal deterioration. Similar expression profiles in the coastal and inland populations suggest comparable genetic control by the microglia and possible similarities in pathogen pressures between habitats. We call for further studies on gene expression of males and females in wild population to understand the implications of immune function for life-histories and demography in natural systems.

Lack of age-related mosaic loss of W chromosome in long-lived birds.

Females and males often exhibit different survival in nature, and it has been hypothesized that sex chromosomes may play a role in driving differential survival rates. For instance, the Y chromosome in mammals and the W chromosome in birds are often degenerated, with reduced numbers of genes, and loss of the Y chromosome in old men is associated with shorter life expectancy. However, mosaic loss of sex chromosomes has not been investigated in any non-human species. Here, we tested whether mosaic loss of the W chromosome (LOW) occurs with ageing in wild birds as a natural consequence of cellular senescence. Using loci-specific PCR and a target sequencing approach we estimated LOW in both young and adult individuals of two long-lived bird species and showed that the copy number of W chromosomes remains constant across age groups. Our results suggest that LOW is not a consequence of cellular ageing in birds. We concluded that the inheritance of the W chromosome in birds, unlike the Y chromosome in mammals, is more stable.

Conserved transcriptomic profiles underpin monogamy across vertebrates.

Social monogamy, typically characterized by the formation of a pair bond, increased territorial defense, and often biparental care, has independently evolved multiple times in animals. Despite the independent evolutionary origins of monogamous mating systems, several homologous brain regions and neuropeptides and their receptors have been shown to play a conserved role in regulating social affiliation and parental care, but little is known about the neuromolecular mechanisms underlying monogamy on a genomic scale. Here, we compare neural transcriptomes of reproductive males in monogamous and nonmonogamous species pairs of Peromyscus mice, Microtus voles, parid songbirds, dendrobatid frogs, and Xenotilapia species of cichlid fishes. We find that, while evolutionary divergence time between species or clades did not explain gene expression similarity, characteristics of the mating system correlated with neural gene expression patterns, and neural gene expression varied concordantly across vertebrates when species transition to monogamy. Our study provides evidence of a universal transcriptomic mechanism underlying the evolution of monogamy in vertebrates.

Transcriptomics of Parental Care in the Hypothalamic-Septal Region of Female Zebra Finch Brain.

(1) Background: The objective of this study was to uncover genomic causes of parental care. Since birds do not lactate and, therefore, do not show the gene expressional changes required for lactation, we investigate gene expression associated with parenting in caring and non-caring females in an avian species, the small passerine bird zebra finch (Taeniopygia guttata). Here, we compare expression patterns in the hypothalamic-septal region since, previously, we showed that this area is activated in parenting females. (2) Methods: Transcriptome sequencing was first applied in a dissected part of the zebra finch brain related to taking care of the nestlings as compared to a control group of social pairs without nestlings. (3) Results: We found genes differentially expressed between caring and non-caring females. When introducing a log2fold change threshold of 1.5, 13 annotated genes were significantly upregulated in breeding pairs, while 39 annotated genes were downregulated. Significant enrichments of dopamine and acetylcholine biosynthetic processes were identified among upregulated pathways, while pro-opiomelanocortin and thyroid hormone pathways were downregulated, suggesting the importance of these systems in parental care. Network analysis further suggested neuro-immunological changes in mothers. (4) Conclusions: The results confirm the roles of several hypothesized major pathways in parental care, whereas novel pathways are also proposed.

The Impact of the COVID-19 Pandemic on Colorectal Cancer Patients in a Tertiary Center in Romania. Single Center Retrospective Study.

Background: The novel coronavirus, SARS-COV-2, was first reported in Wuhan, China in the end of 2019. To curb its spread, social distancing measures and new safety regulations were implemented which led to major disruptions in colorectal cancer care. It is however unknown how it influenced the Romanian colorectal cancer care. Methods and Material: We assessed the demographical, clinical, intraoperative and pathological data of our colorectal cancer patients, 302 in total, between 15.03.2019-14.03.2021. The first year's data was considered as the control group and the second one, the study (pandemic) group. Results: We observed a 12% decrease in colorectal cancer hospitalizations in the first year, 38,6% in the first six months. The rate of emergency admissions, colo/ileostomy formatting procedures, palliative resections, clinical metastasis was higher in the pandemic group. More advanced locoregional invasion, a higher tumor stage, higher rate of vascular, perineural invasion, positive resection margin, and a higher lymph node yield was seen after the restrictions were implemented. Conclusion: The COVID-19 pandemic and the response against it had a major effect on the colorectal cancer care in our country. The outcomes of these worse clinical and pathological findings are unknown, but it is important to do further research in this field. We think colorectal cancer care should have an absolute priority in future pandemics.

Beyond Promoters: How Genes Tweak Their Own Expression.

The correct expression of genes is vital for cells to function. Schikora-Tamarit et al. show that, in addition to obeying their promoters, most genes can modulate their own expression by either buffering or amplification. This could help to avoid costly overexpression of proteins.

Social organization in ungulates: Revisiting Jarman's hypotheses.

Ungulates (antelopes, deer and relatives) have some of the most diverse social systems among mammals. To understand the evolution of ungulate social organization, Jarman (1974) proposed an ecological scenario of how distribution of resources, habitat and feeding style may have influenced social organization. Although Jarman's scenario makes intuitive sense and remains a textbook example of social evolution, it has not been scrutinized using modern phylogenetic comparative methods. Here we use 230 ungulate species from ten families to test Jarman's hypotheses using phylogenetic analyses. Consistent with Jarman's proposition, both habitat and feeding style predict group size, since grazing ungulates typically live in open habitats and form large herds. Group size, in turn, has a knock-on effect on mating systems and sexual size dimorphism, since ungulates that live in large herds exhibit polygamy and extensive sexual size dimorphism. Phylogenetic confirmatory path analyses suggest that evolutionary changes in habitat type, feeding style and body size directly (or indirectly) induce shifts in social organization. Taken together, these phylogenetic comparative analyses confirm Jarman's conjectures, although they also uncover novel relationships between ecology and social organization. Further studies are needed to explore the relevance of Jarman (1974) scenario for mammals beyond ungulates.

Are evolutionary transitions in sexual size dimorphism related to sex determination in reptiles?

Sex determination systems are highly variable in vertebrates, although neither the causes nor the implications of this diversity are fully understood. Theory suggests that sex determination is expected to relate to sexual size dimorphism, because environmental sex determination promotes sex-specific developmental bias in embryonic growth rates. Furthermore, selection for larger size in one sex or the other has been proposed to drive the evolution of different genetic sex determination systems. Here, we investigate whether sex determination systems relate to adult sexual size dimorphism, using 250 species of reptiles (Squamata, Testudines and Crocodylia) representing 26 families. Using phylogenetically informed analyses, we find that sexual size dimorphism is associated with sex determination: species with TSDIa sex determination (i.e. in which the proportion of female offspring increases with incubation temperature) have more female-biased size dimorphism than species with TSDII (i.e. species in which males are produced at mid temperatures). We also found a trend that species with TSD ancestors had more male-biased size dimorphism in XY sex chromosome systems than in ZW sex chromosome systems. Taken together, our results support the prediction that sexual size dimorphism is linked to sex-dependent developmental variations caused by environmental factors and also by sex chromosomes. Since the extent of size dimorphism is related to various behavioural, ecological and life-history differences between sexes, our results imply profound impacts of sex determination systems for vertebrate diversity.

How do biases in sex ratio and disease characteristics affect the spread of sexually transmitted infections?

The epidemiology of sexually transmitted infections (STIs) is inherently linked to host mating dynamics. Studies across many taxa show that adult sex ratio, a major determinant of host mating dynamics, is often skewed - sometimes strongly - toward males or females. However, few predictions exist for the effects of skewed sex ratio on STI epidemiology, and none when coupled with sex biased disease characteristics. Here we use mathematical modelling to examine how interactions between sex ratio and disease characteristics affect STI prevalence in males and females. Notably, we find that while overall disease prevalence peaks at equal sex ratios, prevalence per sex peaks at skewed sex ratios. Furthermore, disease characteristics, sex-biased or not, drive predictable differences in male and female STI prevalence as sex ratio varies, with higher transmission and lower virulence generally increasing differences between the sexes for a given sex ratio. Our work reveals new insights into how STI prevalence in males and females depends on a complex interaction between host population sex ratio and disease characteristics.