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The arrival of agriculture into Europe during the Neolithic transition brought a significant shift in human lifestyle and subsistence. However, the conditions under which the spread of the new culture and technologies occurred are still debated. Similarly, the roles played by women and men during the Neolithic transition are not well understood, probably due to the fact that mitochondrial DNA (mtDNA) and Y chromosome (NRY) data are usually studied independently rather than within the same statistical framework. Here, we applied an integrative approach, using different model-based inferential techniques, to analyse published datasets from contemporary and ancient European populations. By integrating mtDNA and NRY data into the same admixture approach, we show that both males and females underwent the same admixture history and both support the demic diffusion model of Ammerman and Cavalli-Sforza. Similarly, the patterns of genetic diversity found in extant and ancient populations demonstrate that both modern and ancient mtDNA support the demic diffusion model. They also show that population structure and differential growth between farmers and hunter-gatherers are necessary to explain both types of data. However, we also found some differences between male and female markers, suggesting that the female effective population size was larger than that of the males, probably due to different demographic histories. We argue that these differences are most probably related to the various shifts in cultural practices and lifestyles that followed the Neolithic Transition, such as sedentism, the shift from polygyny to monogamy or the increase of patrilocality.

Most methods currently used to infer the “demographic history of species” interpret this expression as a history of population size changes. The detection, quantification, and dating of demographic changes often rely on the assumption that population structure can be neglected. However, most vertebrates are typically organized in populations subdivided into social groups that are usually ignored in the interpretation of genetic data. This could be problematic since an increasing number of studies have shown that population structure can generate spurious signatures of population size change. Here, we simulate microsatellite data from a species subdivided into social groups where reproduction occurs according to different mating systems (monogamy, polygynandry, and polygyny). We estimate the effective population size (Ne) and quantify the effect of social structure on estimates of changes in Ne. We analyze the simulated data with two widely used methods for demographic inference. The first approach, BOTTLENECK, tests whether the samples are at mutation–drift equilibrium and thus whether a single Ne can be estimated. The second approach, msvar, aims at quantifying and dating changes in Ne. We find that social structure may lead to signals of departure from mutation–drift equilibrium including signals of expansion and bottlenecks. We also find that expansion signals may be observed under simple stationary Wright–Fisher models with low diversity. Since small populations tend to characterize many endangered species, we stress that methods trying to infer Ne should be interpreted with care and validated with simulated data incorporating information about structure. Spurious expansion signals due to social structure can mask critical population size changes. These can obscure true bottleneck events and be particularly problematic in endangered species.

Significance Many species live in socially structured populations, forming cohesive units with kin structure. Yet, sociality has been neglected by population geneticists under the assumption that social groups can be seen as small demes subjected to significant genetic drift. Such demes are usually considered to be susceptible to inbreeding, with inbreeding avoidance becoming a major force explaining dispersal strategies. We find that social structure is highly effective in maintaining high genotypic and genetic diversity levels, without invoking sex-biased dispersal or inbreeding avoidance mechanisms. These findings should change the way we perceive social groups. Many species are spatially and socially organized, with complex social organizations and dispersal patterns that are increasingly documented. Social species typically consist of small age-structured units, where a limited number of individuals monopolize reproduction and exhibit complex mating strategies. Here, we model social groups as age-structured units and investigate the genetic consequences of social structure under distinct mating strategies commonly found in mammals. Our results show that sociality maximizes genotypic diversity, which contradicts the belief that social groups are necessarily subject to strong genetic drift and at high risk of inbreeding depression. Social structure generates an excess of genotypic diversity. This is commonly observed in ecological studies but rarely reported in population genetic studies that ignore social structure. This heterozygosity excess, when detected, is often interpreted as a consequence of inbreeding avoidance mechanisms, but we show that it can occur even in the absence of such mechanisms. Many seemly contradictory results from ecology and population genetics can be reconciled by genetic models that include the complexities of social species. We find that such discrepancies can be explained by the intrinsic properties of social groups and by the sampling strategies of real populations. In particular, the number of social groups and the nature of the individuals that compose samples (e.g., nonreproductive and reproductive individuals) are key factors in generating outbreeding signatures. Sociality is an important component of population structure that needs to be revisited by ecologists and population geneticists alike.

The past half century has seen a move from a multiregionalist view of human origins to widespread acceptance that modern humans emerged in Africa. Here the authors argue that a simple out-of-Africa model is also outdated, and that the current state of the evidence favours a structured African metapopulation model of human origins.

Quaternary climatic changes have been invoked as important drivers of species diversification worldwide. However, the impact of such changes on vegetation and animal population dynamics in tropical regions remains debated. To overcome this uncertainty, we integrated high-resolution paleoenvironmental reconstructions from a sedimentary record covering the past 25,000 years with demographic inferences of a forest-dwelling primate species (Microcebus arnholdi), in northern Madagascar. Result comparisons suggest that climate changes through the African Humid Period (15.2 – 5.5 kyr) strongly affected the demographic dynamics of M. arnholdi. We further inferred a population decline in the last millennium which was likely shaped by the combination of climatic and anthropogenic impacts. Our findings demonstrate that population fluctuations in Malagasy wildlife were substantial prior to a significant human impact. This provides a critical knowledge of climatically driven, environmental and ecological changes in the past, which is essential to better understand the dynamics and resilience of current biodiversity.Teixeira et al. combine genomic and palaeoecological datasets to infer the demographic history of a forest-dwelling lemur in Madagascar. Their findings indicate that historical environmental changes drove population demographic changes prior to anthropogenic impact, which was detected in the study region during the last millennium.

Background Iberian primitive breeds exhibit a remarkable phenotypic diversity over a very limited geographical space. While genomic data are accumulating for most commercial cattle, it is still lacking for these primitive breeds. Whole genome data is key to understand the consequences of historic breed formation and the putative role of earlier admixture events in the observed diversity patterns. Results We sequenced 48 genomes belonging to eight Iberian native breeds and found that the individual breeds are genetically very distinct with F ST values ranging from 4 to 16% and have levels of nucleotide diversity similar or larger than those of their European counterparts, namely Jersey and Holstein. All eight breeds display significant gene flow or admixture from African taurine cattle and include mtDNA and Y-chromosome haplotypes from multiple origins. Furthermore, we detected a very low differentiation of chromosome X relative to autosomes within all analyzed taurine breeds, potentially reflecting male-biased gene flow. Conclusions Our results show that an overall complex history of admixture resulted in unexpectedly high levels of genomic diversity for breeds with seemingly limited geographic ranges that are distantly located from the main domestication center for taurine cattle in the Near East. This is likely to result from a combination of trading traditions and breeding practices in Mediterranean countries. We also found that the levels of differentiation of autosomes vs sex chromosomes across all studied taurine and indicine breeds are likely to have been affected by widespread breeding practices associated with male-biased gene flow.

Background Quaternary climate fluctuations have been acknowledged as major drivers of the geographical distribution of the extraordinary biodiversity observed in tropical biomes, including Madagascar. The main existing framework for Pleistocene Malagasy diversification assumes that forest cover was strongly shaped by warmer Interglacials (leading to forest expansion) and by cooler and arid glacials (leading to forest contraction), but predictions derived from this scenario for forest-dwelling animals have rarely been tested with genomic datasets. Results We generated genomic data and applied three complementary demographic approaches ( Stairway Plot , PSMC and IICR -simulations) to infer population size and connectivity changes for two forest-dependent primate species ( Microcebus murinus and M. ravelobensis ) in northwestern Madagascar. The analyses suggested major demographic changes in both species that could be interpreted in two ways, depending on underlying model assumptions (i.e., panmixia or population structure). Under panmixia, the two species exhibited larger population sizes across the Last Glacial Maximum (LGM) and towards the African Humid Period (AHP). This peak was followed by a population decline in M. ravelobensis until the present, while M. murinus may have experienced a second population expansion that was followed by a sharp decline starting 3000 years ago. In contrast, simulations under population structure suggested decreasing population connectivity between the Last Interglacial and the LGM for both species, but increased connectivity during the AHP exclusively for M. murinus . Conclusion Our study shows that closely related species may differ in their responses to climatic events. Assuming that Pleistocene climatic conditions in the lowlands were similar to those in the Malagasy highlands, some demographic dynamics would be better explained by changes in population connectivity than in population size. However, changes in connectivity alone cannot be easily reconciled with a founder effect that was shown for M. murinus during its colonization of the northwestern Madagascar in the late Pleistocene. To decide between the two alternative models, more knowledge about historic forest dynamics in lowland habitats is necessary. Altogether, our study stresses that demographic inferences strongly depend on the underlying model assumptions. Final conclusions should therefore be based on a comparative evaluation of multiple approaches.

The western chimpanzee (Pan troglodytes verus) is a Critically Endangered taxon. In Guinea‐Bissau (GB), the subspecies is increasingly threatened, but there is a lack of understanding regarding the degree of genetic threat faced by populations. This hinders the development of targeted conservation strategies and the prioritization of efforts by national agencies. In this study, we use microsatellite data from four parks located in southern GB and five whole‐genome sequences to estimate the effective population size (Ne) and infer the recent and ancient demographic history of populations using different methods. We also aim to integrate the different Ne estimates to improve our understanding of the evolutionary history and current demography of this great ape and to discuss the strengths and limitations of each estimator and their complementarity in informing conservation decisions. Results from the PSMC method suggest a large ancestral Ne, likely due to ancient structure over the whole subspecies distribution until approximately 10,000–15,000 years ago. After that, a change in connectivity, a real decrease in size, or a combination of both occurred, which reduced the then still large ancestral population to a smaller size (MSVAR: ~10,000 decreasing to 1,000–6,000 breeding individuals), possibly indicating a fragmentation into coastal and inland subpopulations. In the most recent past, contemporary Ne is close to 500 (GONE: 395–583, NeEstimator: 107–549), suggesting a high risk of extinction. The populations located at the coastal parks may have been small or isolated for several generations and are at higher risk, whereas the ones located inland exhibit higher long‐term Ne and can be considered a stronghold for chimpanzee conservation. Through combining different types of molecular markers and analytical methodologies, we tried to overcome the limitations of obtaining high‐quality DNA samples from wild threatened populations and estimated Ne at different temporal and spatial scales, which is crucial information to make informed conservation decisions at local and regional scales.

A Correction to this paper has been published: https://doi.org/10.1038/s41437-021-00414-z

Great ape populations are undergoing a dramatic decline, which is predicted to result in their extinction in the wild from entire regions in the near future. Recent findings have particularly focused on African apes, and have implicated multiple factors contributing to this decline, such as deforestation, hunting, and disease. Less well-publicised, but equally dramatic, has been the decline in orang-utans, whose distribution is limited to parts of Sumatra and Borneo. Using the largest-ever genetic sample from wild orang-utan populations, we show strong evidence for a recent demographic collapse in North Eastern Borneo and demonstrate that this signature is independent of the mutation and demographic models used. This is the first demonstration that genetic data can detect and quantify the effect of recent, human-induced deforestation and habitat fragmentation on an endangered species. Because current demographic collapses are usually confounded by ancient events, this suggests a much more dramatic decline than demographic data alone and emphasises the need for major conservation efforts.