The effect of divergent and parallel selection on the genomic landscape of divergence.

While the role of selection in divergence along the speciation continuum is theoretically well understood, defining specific signatures of selection in the genomic landscape of divergence is empirically challenging. Modelling approaches can provide insight into the potential role of selection on the emergence of a heterogenous genomic landscape of divergence. Here, we extend and apply an individual-based approach that simulates the phenotypic and genotypic distributions of two populations under a variety of selection regimes, genotype-phenotype maps, modes of migration, and genotype-environment interactions. We show that genomic islands of high differentiation and genomic valleys of similarity may respectively form under divergent and parallel selection between populations. For both types of between-population selection, negative and positive frequency-dependent selection within populations generated genomic islands of higher magnitude and genomic valleys of similarity, respectively. Divergence rates decreased under strong dominance with divergent selection, as well as in models including genotype-environment interactions under parallel selection. For both divergent and parallel selection models, divergence rate was higher under an intermittent migration regime between populations, in contrast to a constant level of migration across generations, despite an equal number of total migrants. We highlight that interpreting a particular evolutionary history from an observed genomic pattern must be done cautiously, as similar patterns may be obtained from different combinations of evolutionary processes. Modelling approaches such as ours provide an opportunity to narrow the potential routes that generate the genomic patterns of specific evolutionary histories.

Benchmarking the Mantel test and derived methods for testing association between distance matrices.

Testing the association between objects is central in ecology, evolution, and quantitative sciences in general. Two types of variables can describe the relationships between objects: point variables (measured on individual objects), and distance variables (measured between pairs of objects). The Mantel test and derived methods have been extensively used for distance variables. Yet, these methods have been criticized due to low statistical power and inflated type I error when spatial autocorrelation is present. Here, we assessed the statistical power between different types of tested variables and the type I error rate over a wider range of autocorrelation intensities than previously assessed, both on univariate and multivariate data. We also illustrated the performance of distance matrix statistics through computational simulations of genetic diversity. We show that the Mantel test and derived methods are not affected by inflated type I error when spatial autocorrelation affects only one variable when investigating correlations, or when either the response or the explanatory variable(s) is affected by spatial autocorrelation while investigating causal relationships. As previously noted, with autocorrelation affecting more variables, inflated type I error could be reduced by modifying the significance threshold. Additionally, the Mantel test has no problem of statistical power when the hypothesis is formulated in terms of distance variables. We highlight that transformation of variable types should be avoided because of the potential information loss and modification of the tested hypothesis. We propose a set of guidelines to help choose the appropriate method according to the type of variables and defined hypothesis.

Temporal Variation in Introgressed Segments' Length Statistics Computed from a Limited Number of Ancient Genomes Sheds Light on Past Admixture Pulses.

Hybridization is recognized as an important evolutionary force, but identifying and timing admixture events between divergent lineages remain a major aim of evolutionary biology. While this has traditionally been done using inferential tools on contemporary genomes, the latest advances in paleogenomics have provided a growing wealth of temporally distributed genomic data. Here, we used individual-based simulations to generate chromosome-level genomic data for a 2-population system and described temporal neutral introgression patterns under a single- and 2-pulse admixture model. We computed 6 summary statistics aiming to inform the timing and number of admixture pulses between interbreeding entities: lengths of introgressed sequences and their variance within genomes, as well as genome-wide introgression proportions and related measures. The first 2 statistics could confidently be used to infer interlineage hybridization history, peaking at the beginning and shortly after an admixture pulse. Temporal variation in introgression proportions and related statistics provided more limited insights, particularly when considering their application to ancient genomes still scant in number. Lastly, we computed these statistics on Homo sapiens paleogenomes and successfully inferred the hybridization pulse from Neanderthal that occurred approximately 40 to 60 kya. The scarce number of genomes dating from this period prevented more precise inferences, but the accumulation of paleogenomic data opens promising perspectives as our approach only requires a limited number of ancient genomes.

Past human expansions shaped the spatial pattern of Neanderthal ancestry.

The worldwide expansion of modern humans (Homo sapiens) started before the extinction of Neanderthals (Homo neanderthalensis). Both species coexisted and interbred, leading to slightly higher introgression in East Asians than in Europeans. This distinct ancestry level has been argued to result from selection, but range expansions of modern humans could provide an alternative explanation. This hypothesis would lead to spatial introgression gradients, increasing with distance from the expansion source. We investigate the presence of Neanderthal introgression gradients after past human expansions by analyzing Eurasian paleogenomes. We show that the out-of-Africa expansion resulted in spatial gradients of Neanderthal ancestry that persisted through time. While keeping the same gradient orientation, the expansion of early Neolithic farmers contributed decisively to reducing the Neanderthal introgression in European populations compared to Asian populations. This is because Neolithic farmers carried less Neanderthal DNA than preceding Paleolithic hunter-gatherers. This study shows that inferences about past human population dynamics can be made from the spatiotemporal variation in archaic introgression.

Survival rates in the world's southernmost forest bird community.

The Magellanic sub-Antarctic Forest is home to the world's southernmost avian community and is the only Southern Hemisphere analogue to Northern Hemisphere temperate forests at this latitude. This region is considered among the few remaining pristine areas of the world, and shifts in environmental conditions are predominantly driven by climate variability. Thus, understanding climate-driven demographic processes is critical for addressing conservation issues in this system under future climate change scenarios. Here, we describe annual survival patterns and their association with climate variables using a 20-year mark-recapture data set of five forest bird species in the Cape Horn Biosphere Reserve. We develop a multispecies hierarchical survival model to jointly explore age-dependent survival probabilities at the community and species levels in a group of five forest passerines. At the community level, we assess the association of migratory behavior and body size with survival, and at the species level, we investigate the influence of local and regional climatic variables on temporal variations of survival. We found a positive effect of precipitation and a negative effect of El Niño Southern Oscillation on juvenile survival in the white-crested Elaenia and a consistent but uncertain negative effect of temperature on survival in juveniles and 80% of adults. We found only a weak association of climate variables with survival across species in the community and no temporal trends in survival for any of the species in either age class, highlighting apparent stability in these high austral latitude forests. Finally, our findings provide an important resource of survival probabilities, a necessary input for assessing potential impacts of global climate change in this unique region of the world.

The Subantarctic Rayadito (Aphrastura subantarctica), a new bird species on the southernmost islands of the Americas.

We describe a new taxon of terrestrial bird of the genus Aphrastura (rayaditos) inhabiting the Diego Ramírez Archipelago, the southernmost point of the American continent. This archipelago is geographically isolated and lacks terrestrial mammalian predators as well as woody plants, providing a contrasted habitat to the forests inhabited by the other two Aphrastura spp. Individuals of Diego Ramírez differ morphologically from Aphrastura spinicauda, the taxonomic group they were originally attributed to, by their larger beaks, longer tarsi, shorter tails, and larger body mass. These birds move at shorter distances from ground level, and instead of nesting in cavities in trees, they breed in cavities in the ground, reflecting different life-histories. Both taxa are genetically differentiated based on mitochondrial and autosomal markers, with no evidence of current gene flow. Although further research is required to define how far divergence has proceeded along the speciation continuum, we propose A. subantarctica as a new taxonomic unit, given its unique morphological, genetic, and behavioral attributes in a non-forested habitat. The discovery of this endemic passerine highlights the need to monitor and conserve this still-pristine archipelago devoid of exotic species, which is now protected by the recently created Diego Ramírez Islands-Drake Passage Marine Park.

The extreme rainfall gradient of the Cape Horn Biosphere Reserve and its impact on forest bird richness.

A natural laboratory is a place supporting the conditions for hypothesis testing under non-anthropogenic settings. Located at the southern end of the Magellanic sub-Antarctic ecoregion in southwestern South America, the Cape Horn Biosphere Reserve (CHBR) has one of the most extreme rainfall gradients in the world. Subject to oceanic climate conditions, it is also characterized by moderate thermal fluctuations throughout the year. This makes it a unique natural laboratory for studying the effects of extreme rainfall variations on forest bird communities. Here, we monitor the bird species richness in the different forest types present in the CHBR. We found that species richness decreased with increasing precipitation, in which an increase of 100 mm in average annual precipitation showed about 1% decrease in species richness. Similar patterns were found among different forest types within the CHBR. These results provide a baseline to investigate the interactions between physical and biotic factors in a subpolar region that climatically contrasts with boreal forests, which is subject to continental climatic conditions. This research highlights the importance of ecological and ornithological long-term studies in the CHBR, which can contribute both to a higher resolution of the heterogeneity of climate changes in different regions of the world, and to orient conservation policies in the Magellanic sub-Antarctic ecoregion in the face of growing development pressures.

The wild ancestors of domestic animals as a neglected and threatened component of biodiversity.

Domestic animals have immense economic, cultural, and practical value and have played pivotal roles in the development of human civilization. Many domesticates have, among their wild relatives, undomesticated forms representative of their ancestors. Resurgent interest in these ancestral forms has highlighted the unclear genetic status of many, and some are threatened with extinction by hybridization with domestic conspecifics. We considered the contemporary status of these ancestral forms relative to their scientific, practical, and ecological importance; the varied impacts of wild-domestic hybridization; and the challenges and potential resolutions involved in conservation efforts. Identifying and conserving ancestral forms, particularly with respect to disentangling patterns of gene flow from domesticates, is complex because of the lack of available genomic and phenotypic baselines. Comparative behavioral, ecological, and genetic studies of ancestral-type, feral, and domestic animals should be prioritized to establish the contemporary status of the former. Such baseline information will be fundamental in ensuring successful conservation efforts.

Los Ancestros de Animales Domésticos como un Componente Descuidado y Amenazado de la Biodiversidad Resumen Los animales domésticos tienen un inmenso valor económico, cultural y práctico y han jugado un papel muy importante en el desarrollo de la civilización humana. Muchos animales domesticados tienen, entre sus parientes silvestres, formas no domesticadas representativas de sus ancestros. Un interés renovado en estas formas ancestarles ha destacado el estatus genético poco claro de muchas, y algunas están amenazadas de extinción por hibridación con conespecíficos domesticados. Consideramos el estatus contempóraneo de estas formas ancestrales en relación con su importancia científica, práctica y ecológica; los impactos diversos de la hibridación silvestre-domesticado; y los retos y soluciones potenciales involucrados en los esfuerzos de conservación. La identificación y conservación de formas ancestrales, particularmente en relación con desenredar patrones de flujo génicos, es compleja debido a la carencia de líneas de base genómicas y fenotípicas. Se deben priorizar estudios conductuales, ecológicos y genéticos comparativos de los animales ancestrales, ferales y domésticos para establecer el estatus contemporáno de los primeros. Tal información de base será fundamental para asegurar esfuerzos de conservación exitosos.

Spatially explicit paleogenomic simulations support cohabitation with limited admixture between Bronze Age Central European populations.

The Bronze Age is a complex period of social, cultural and economic changes. Recent paleogenomic studies have documented a large and rapid genetic change in early Bronze Age populations from Central Europe. However, the detailed demographic and genetic processes involved in this change are still debated. Here we have used spatially explicit simulations of genomic components to better characterize the demographic and migratory conditions that may have led to this change. We investigated various scenarios representing the expansion of pastoralists from the Pontic steppe, potentially linked to the Yamnaya cultural complex, and their interactions with local populations in Central Europe, considering various eco-evolutionary factors, such as population admixture, competition and long-distance dispersal. Our results do not support direct competition but rather the cohabitation of pastoralists and farmers in Central Europe, with limited gene flow between populations. They also suggest occasional long-distance migrations accompanying the expansion of pastoralists and a demographic decline in both populations following their initial contact. These results link recent archaeological and paleogenomic observations and move further the debate of genomic changes during the early Bronze Age.

Air temperature influences early Covid-19 outbreak as indicated by worldwide mortality.

The Covid-19 outbreak has triggered a global crisis that is challenging governments, health systems and the scientific community worldwide. A central question in the Covid-19 pandemic is whether climatic factors have influenced its progression. To address this question, we used mortality rates during the first three weeks of recorded mortality in 144 countries, during the first wave of the pandemic. We examined the effect of climatic variables, along with the proportion of the population older than 64 years old, the number of beds in hospitals, and the timing and strength of the governmental travel measures to control the spread of the disease. Our first model focuses on air temperature as the central climatic factor and explains 67% of the variation in mortality rate, with 37% explained by the fixed variables considered and 31% explained by country-specific variations. We show that mortality rate is negatively influenced by warmer air temperature. Each additional Celsius degree decreases mortality rate by ~5%. Our second model is centred on the UV Index and follows the same trend as air temperature, explaining 69% of the variation in mortality rate. These results are robust to the exclusion of countries with low incomes, as well as to the exclusion of low- and medium-income countries. We also show that the proportion of vulnerable age classes and access to healthcare are critical factors impacting the mortality rate of this disease. The effects of air temperature at an early stage of the Covid-19 outbreak is a key factor to understand the primary spread of this pandemic, and should be considered in projecting subsequent waves.

Projecting introgression from domestic cats into European wildcats in the Swiss Jura.

Hybridization between wild and domesticated organisms is a worldwide conservation issue. In the Jura Mountains, threatened European wildcats (Felis silvestris) have been demographically spreading for approximately the last 50 years, but this recovery is coupled with hybridization with domestic cats (Felis catus). Here, we project the pattern of future introgression using different spatially explicit scenarios to model the interactions between the two species, including competition and different population sizes. We project the fast introgression of domestic cat genes into the wildcat population under all scenarios if hybridization is not severely restricted. If the current hybridization rate and population sizes remain unchanged, we expect the loss of genetic distinctiveness between wild and domestic cats at neutral nuclear, mitochondrial and Y chromosome markers in one hundred years. However, scenarios involving a competitive advantage for wildcats and a future increase in the wildcat population size project a slower increase in introgression. We recommend that future studies assess the fitness of these hybrids and better characterize their ecological niche and their ecological interactions with parental species to elucidate effective conservation measures.

Harmonizing hybridization dissonance in conservation.

A dramatic increase in the hybridization between historically allopatric species has been induced by human activities. However, the notion of hybridization seems to lack consistency in two respects. On the one hand, it is inconsistent with the biological species concept, which does not allow for interbreeding between species, and on the other hand, it is considered either as an evolutionary process leading to the emergence of new biodiversity or as a cause of biodiversity loss, with conservation implications. In the first case, we argue that conservation biology should avoid the discussion around the species concept and delimit priorities of conservation units based on the impact on biodiversity if taxa are lost. In the second case, we show that this is not a paradox but an intrinsic property of hybridization, which should be considered in conservation programmes. We propose a novel view of conservation guidelines, in which human-induced hybridization may also be a tool to enhance the likelihood of adaptation to changing environmental conditions or to increase the genetic diversity of taxa affected by inbreeding depression. The conservation guidelines presented here represent a guide for the development of programmes aimed at protecting biodiversity as a dynamic evolutionary system.

The Genomic Landscape of Divergence Across the Speciation Continuum in Island-Colonising Silvereyes (Zosterops lateralis).

Inferring the evolutionary dynamics at play during the process of speciation by analyzing the genomic landscape of divergence is a major pursuit in population genomics. However, empirical assessments of genomic landscapes under varying evolutionary scenarios that are known a priori are few, thereby limiting our ability to achieve this goal. Here we combine RAD-sequencing and individual-based simulations to evaluate the genomic landscape of divergence in the silvereye (Zosterops lateralis). Using pairwise comparisons that differ in divergence timeframe and the presence or absence of gene flow, we document how genomic patterns accumulate along the speciation continuum. In contrast to previous predictions, our results provide limited support for the idea that divergence accumulates around loci under divergent selection or that genomic islands widen with time. While a small number of genomic islands were found in populations diverging with and without gene flow, in few cases were SNPs putatively under selection tightly associated with genomic islands. The transition from localized to genome-wide levels of divergence was captured using individual-based simulations that considered only neutral processes. Our results challenge the ubiquity of existing verbal models that explain the accumulation of genomic differences across the speciation continuum and instead support the idea that divergence both within and outside of genomic islands is important during the speciation process.

SPLATCHE3: simulation of serial genetic data under spatially explicit evolutionary scenarios including long-distance dispersal.

SUMMARY: SPLATCHE3 simulates genetic data under a variety of spatially explicit evolutionary scenarios, extending previous versions of the framework. The new capabilities include long-distance migration, spatially and temporally heterogeneous short-scale migrations, alternative hybridization models, simulation of serial samples of genetic data and a large variety of DNA mutation models. These implementations have been applied independently to various studies, but grouped together in the current version. AVAILABILITY AND IMPLEMENTATION: SPLATCHE3 is written in C++ and is freely available for non-commercial use from the website http://www.splatche.com/splatche3. It includes console versions for Linux, MacOs and Windows and a user-friendly GUI for Windows, as well as detailed documentation and ready-to-use examples.

Hybridization and introgression during density-dependent range expansion: European wildcats as a case study.

Interbreeding between historically allopatric species with incomplete reproductive barriers may result when species expand their range. The genetic consequences of such hybridization depend critically on the dynamics of the range expansion. Hybridization models during range expansion have been developed but assume dispersal to be independent from neighboring population densities. However, organisms may disperse because they are attracted by conspecifics or because they prefer depopulated areas. Here, through spatially explicit simulations, we assess the effect of various density-dependent dispersal modes on the introgression between two species. We find huge introgression from the local species into the invasive one with all dispersal modes investigated, even when the hybridization rate is relatively low. This represents a general expectation for neutral genes even if the dispersal modes differ in colonization times and amount of introgression. Invasive individuals attracted by conspecifics need more time to colonize the whole area and are more introgressed by local genes, whereas the opposite is found for solitary individuals. We applied our approach to a recent expansion of European wildcats in the Jura Mountains and the hybridization with domestic cats. We show that the simulations explained better the observed level of introgression at nuclear, mtDNA, and Y chromosome markers, when using solitary dispersal for wildcats instead of random or gregarious dispersal, in accordance with ecological knowledge. Thus, use of density-dependent dispersal models increases the predictive power of the approach.

Effect of hybridization with genome exclusion on extinction risk.

Human-induced habitat changes may lead to the breakdown of reproductive barriers between distantly related species. This phenomenon may result in fertile first-generation hybrids (F1 ) that exclude the genome of one parental species during gametogenesis, thus disabling introgression. The species extinction risk associated with hybridization with genome exclusion is largely underappreciated because the phenomenon produces only F1 hybrid phenotype, leading to the misconception that hybrids are sterile and potentially of minor conservation concern. We used a simulation model that integrates the main genetic, demographic, and ecological processes to examine the dynamics of hybridization with genome exclusion. We showed that this mode of hybridization may lead to extremely rapid extinction when the process of genome exclusion is unbalanced between the interbreeding species and when the hybridization rate is not negligible. The coexistence of parental species was possible in some cases of asymmetrical genome exclusion, but show this equilibrium was highly vulnerable to environmental variation. Expanding the exclusive habitat of the species at risk allowed its persistence. Our results highlight the extent of possible extinction risk due to hybridization with genome exclusion and suggest habitat management as a promising conservation strategy. In anticipation of serious threats to biodiversity due to hybridization with genome exclusion, we recommend a detailed assessment of the reproductive status of hybrids in conservation programs. We suggest such assessments include the inspection of genetic content in hybrid gametes.

Cryptic Biological Invasions: a General Model of Hybridization.

The dispersal of non-native genes due to hybridization is a form of cryptic invasion with growing concern in evolution and conservation. This includes the spread of transgenic genes and antibiotic resistance. To investigate how genes and phenotypes are transmitted, we developed a general model that, for the first time, considers concurrently: multiple loci, quantitative and qualitative gene expression, assortative mating, dominance/recessivity inheritance and density-dependent demographic effects. Selection acting on alleles or genotypes can also be incorporated. Our results reveal that the conclusions about how hybridization threatens a species can be biased if they are based on single-gene models, while considering two or more genes can correct this bias. We also show that demography can amplify or balance the genetic effects, evidencing the need of jointly incorporating both processes. By implementing our model in a real case, we show that mallard ducks introduced in New Zealand benefit from hybridization to replace native grey-ducks. Total displacement can take a few generations and occurs by interspecific competition and by competition between hybrids and natives, demonstrating how hybridization may facilitate biological invasions. We argue that our general model represents a powerful tool for the study of a wide range of biological and societal questions.

Modelling interspecific hybridization with genome exclusion to identify conservation actions: the case of native and invasive Pelophylax waterfrogs.

Interspecific hybridization occurs in nature but can also be caused by human actions. It often leads to infertile or fertile hybrids that exclude one parental genome during gametogenesis, escaping genetic recombination and introgression. The threat that genome-exclusion hybridization might represent on parental species is poorly understood, especially when invasive species are involved. Here, we show how to assess the effects of genome-exclusion hybridization and how to elaborate conservation actions by simulating scenarios using a model of nonintrogressive hybridization. We examine the case of the frog Pelophylax ridibundus, introduced in Western Europe, which can hybridize with the native Pelophylax lessonae and the pre-existing hybrid Pelophylax esculentus, maintained by hybridogenesis. If translocated from Southern Europe, P. ridibundus produces new sterile hybrids and we show that it mainly threatens P. esculentus. Translocation from Central Europe leads to new fertile hybrids, threatening all native waterfrogs. Local extinction is demographically mediated via wasted reproductive potential or via demographic flow through generations towards P. ridibundus. We reveal that enlarging the habitat size of the native P. lessonae relative to that of the invader is a promising conservation strategy, avoiding the difficulties of fighting the invader. We finally stress that nonintrogressive hybridization is to be considered in conservation programmes.

A general model of distant hybridization reveals the conditions for extinction in Atlantic salmon and brown trout.

Interspecific hybridization is common in nature but can be increased in frequency or even originated by human actions, such as species introduction or habitat modification, which may threaten species persistence. When hybridization occurs between distantly related species, referred to as "distant hybridization," the resulting hybrids are generally infertile or fertile but do not undergo chromosomal recombination during gametogenesis. Here, we present a model describing this frequent but poorly studied interspecific hybridization to assess its consequences on parental species and to anticipate the conditions under which they can reach extinction. Our general model fully incorporates three important processes: density-dependent competition, dominance/recessivity inheritance of traits and assortative mating. We demonstrate its use and flexibility by assessing population extinction risk between Atlantic salmon and brown trout in Norway, whose interbreeding has recently increased due to farmed fish releases into the wild. We identified the set of conditions under which hybridization may threaten salmonid species. Thanks to the flexibility of our model, we evaluated the effect of an additional risk factor, a parasitic disease, and showed that the cumulative effects dramatically increase the extinction risk. The consequences of distant hybridization are not genetically, but demographically mediated. Our general model is useful to better comprehend the evolution of such hybrid systems and we demonstrated its importance in the field of conservation biology to set up management recommendations when this increasingly frequent type of hybridization is in action.