David Díez-del-Molino

Early farmers from across Europe directly descended from Neolithic Aegeans

Significance One of the most enduring and widely debated questions in prehistoric archaeology concerns the origins of Europe’s earliest farmers: Were they the descendants of local hunter-gatherers, or did they migrate from southwestern Asia, where farming began? We recover genome-wide DNA sequences from early farmers on both the European and Asian sides of the Aegean to reveal an unbroken chain of ancestry leading from central and southwestern Europe back to Greece and northwestern Anatolia. Our study provides the coup de grâce to the notion that farming spread into and across Europe via the dissemination of ideas but without, or with only a limited, migration of people. Farming and sedentism first appeared in southwestern Asia during the early Holocene and later spread to neighboring regions, including Europe, along multiple dispersal routes. Conspicuous uncertainties remain about the relative roles of migration, cultural diffusion, and admixture with local foragers in the early Neolithization of Europe. Here we present paleogenomic data for five Neolithic individuals from northern Greece and northwestern Turkey spanning the time and region of the earliest spread of farming into Europe. We use a novel approach to recalibrate raw reads and call genotypes from ancient DNA and observe striking genetic similarity both among Aegean early farmers and with those from across Europe. Our study demonstrates a direct genetic link between Mediterranean and Central European early farmers and those of Greece and Anatolia, extending the European Neolithic migratory chain all the way back to southwestern Asia.

Early Neolithic genomes from the eastern Fertile Crescent

Near Eastern genomes from Iran The genetic composition of populations in Europe changed during the Neolithic transition from hunting and gathering to farming. To better understand the origin of modern populations, Broushaki et al. sequenced ancient DNA from four individuals from the Zagros region of present-day Iran, representing the early Neolithic Fertile Crescent. These individuals unexpectedly were not ancestral to early European farmers, and their genetic structures did not contribute significantly to those of present-day Europeans. These data indicate that a parallel Neolithic transition probably resulted from structured farming populations across southwest Asia. Science, this issue p. 499 Neolithic people from the region of modern Iran are genetically distinct from early northwestern Anatolian and European farmers. We sequenced Early Neolithic genomes from the Zagros region of Iran (eastern Fertile Crescent), where some of the earliest evidence for farming is found, and identify a previously uncharacterized population that is neither ancestral to the first European farmers nor has contributed substantially to the ancestry of modern Europeans. These people are estimated to have separated from Early Neolithic farmers in Anatolia some 46,000 to 77,000 years ago and show affinities to modern-day Pakistani and Afghan populations, but particularly to Iranian Zoroastrians. We conclude that multiple, genetically differentiated hunter-gatherer populations adopted farming in southwestern Asia, that components of pre-Neolithic population structure were preserved as farming spread into neighboring regions, and that the Zagros region was the cradle of eastward expansion.

Gene flow and maintenance of genetic diversity in invasive mosquitofish (Gambusia holbrooki).

Genetic analyses contribute to studies of biological invasions by mapping the origin and dispersal patterns of invasive species occupying new territories. Using microsatellite loci, we assessed the genetic diversity and spatial population structure of mosquitofish (Gambusia holbrooki) that had invaded Spanish watersheds, along with the American locations close to the suspected potential source populations. Mosquitofish populations from the Spanish streams that were studied had similar levels of genetic diversity to the American samples; therefore, these populations did not appear to have undergone substantial losses of genetic diversity during the invasion process. Population structure analyses indicated that the Spanish populations fell into four main clusters, which were primarily associated with hydrography. Dispersal patterns indicated that local populations were highly connected upstream and downstream through active dispersal, with an average of 21.5% fish from other locations in each population. After initially introducing fish to one location in a given basin, such dispersal potential might contribute to the spread and colonization of suitable habitats throughout the entire river basin. The two-dimension isolation-by-distance pattern here obtained, indicated that the human-mediated translocation of mosquitofish among the three study basins is a regular occurrence. Overall, both phenomena, high natural dispersal and human translocation, favor gene flow among river basins and the retention of high genetic diversity, which might help retain the invasive potential of mosquitofish populations.

Genetic characterization of the invasive mosquitofish (Gambusia spp.) introduced to Europe: Population structure and colonization routes

Biological invasions are considered one of the main anthropogenic factors that reduce the abundance of native species. Understanding the patterns of population structure and behavior of introduced species is important to determine invasion sources and pathways, in addition to improving the protective management of native species. Thus, we set out to advance our knowledge about the mosquitofish Gambusia spp., which is an invasive species that was introduced to southern Europe in 1921 to control mosquito populations. We assessed the genetic diversity and population structure of this species at 13 European locations, by screening variation at six microsatellite loci. We also evaluated six American samples (four of G. holbrooki and two of G. affinis) to identify the most likely source of the populations that established in Europe, and to determine whether G. affinis is also present. The results showed that, while there was evidence of recent bottleneck events in a few isolated locations, most introduced populations harbored a considerable amount of gene diversity, probably because of multiple introductions and secondary contacts. Populations displayed strong genetic differentiation that was mainly associated with geographical distance. At least two main routes of colonization of G. holbrooki seem to have occurred in Europe. The first, and more ancient colonization, was consistent with historical records, with the species invading the Iberian Peninsula. A second and more recent colonization probably occurred in Greece and, from there, France. The presence of G. affinis was not detected in any of the European samples.

Genomic survey provides insights into the evolutionary changes that occurred during European expansion of the invasive mosquitofish (Gambusia holbrooki)

Biological invasions rank among the main global threats for biodiversity. The Eastern mosquitofish (Gambusia holbrooki) is considered one of the 100 world worst invasive species due to its high adaptation capability to new environments. Using the restriction‐site‐associated DNA tags (RADtags), introduced European locations were compared against native US mosquitofish populations to analyse genomic changes that occurred during invasive process of European locations. After filtering, 7724 RADtags containing only one SNP were retained for population studies. Comparative genomics indicated that 186 of these RADtags matched sequences in the transcriptome of Xyphophorus maculatus, the most closely related genome available. Genomic analyses showed that invasive populations show high reductions in diversity. Further, analyses of population structuring based on these data are concordant with previous analyses based on microsatellites. It is concluded that during the invasion process genetic drift was the main evolutionary force affecting patterns of diversity and population structure. While recognizing that positive selection could be masked by the strong drift during founder events, adaptive processes were evidenced in a reduced number of RADtags (<2%), with only one of these in a putative coding region. Surprisingly, balancing selection was detected in several coding RADtags, suggesting that the preservation of polymorphism in specific genes could be more important than the average population diversity for the population maintenance at any location, particularly for the survival of introduced populations.

Quantifying Temporal Genomic Erosion in Endangered Species

Many species have undergone dramatic population size declines over the past centuries. Although stochastic genetic processes during and after such declines are thought to elevate the risk of extinction, comparative analyses of genomic data from several endangered species suggest little concordance between genome-wide diversity and current population sizes. This is likely because species-specific life-history traits and ancient bottlenecks overshadow the genetic effect of recent demographic declines. Therefore, we advocate that temporal sampling of genomic data provides a more accurate approach to quantify genetic threats in endangered species. Specifically, genomic data from predecline museum specimens will provide valuable baseline data that enable accurate estimation of recent decreases in genome-wide diversity, increases in inbreeding levels, and accumulation of deleterious genetic variation.

Changes in variation at the MHC class II DQA locus during the final demise of the woolly mammoth.

According to the nearly-neutral theory of evolution, the relative strengths of selection and drift shift in favour of drift at small population sizes. Numerous studies have analysed the effect of bottlenecks and small population sizes on genetic diversity in the MHC, which plays a central role in pathogen recognition and immune defense and is thus considered a model example for the study of adaptive evolution. However, to understand changes in genetic diversity at loci under selection, it is necessary to compare the genetic diversity of a population before and after the bottleneck. In this study, we analyse three fragments of the MHC DQA gene in woolly mammoth samples radiocarbon dated to before and after a well-documented bottleneck that took place about ten thousand years ago. Our results indicate a decrease in observed heterozygosity and number of alleles, suggesting that genetic drift had an impact on the variation on MHC. Based on coalescent simulations, we found no evidence of balancing selection maintaining MHC diversity during the Holocene. However, strong trans-species polymorphism among mammoths and elephants points to historical effects of balancing selection on the woolly mammoth lineage.

Multiple paternity and reproduction opportunities for invasive mosquitofish

The American mosquitofish, Gambusia holbrooki, is a worldwide invasive species. Multiple paternity might contribute to the invasive success of this species, by locally increasing effective population size. Using microsatellite loci, we examined multiple paternity of mosquitofish in Spanish basins. The percentage of gravid females that mated multiple times (greater than 60%), the average brood size (13.2), and the average number of sires per female brood (3–4) in the invaded basins were similar to values reported in America. Partial correlation showed that female size was not related to the number of sires independent of brood size. In addition, positive correlations between female size and the effective number of sires, or the reproductive skew were dependent on brood size. A relevant percentage of females mating with more than 3 sires suggested enhanced opportunities for transmission of diversity to subsequent generations in Spanish populations. Within broods, a dominant male often sired half of the brood. These results suggest multiple paternity is common in invaded populations. Together with known reproductive tactics of mosquitofish giving to any mature individual the chance for mating regardless of size or age, possibly multiple paternity facilitate the persistence of the genetic diversity of local populations.

Mitogenome evolution in the last surviving woolly mammoth population reveals neutral and functional consequences of small population size

The onset of the Holocene was associated with a global temperature increase, which led to a rise in sea levels and isolation of the last surviving population of woolly mammoths on Wrangel Island. Understanding what happened with the populations genetic diversity at the time of the isolation and during the ensuing 6000 years can help clarify the effects of bottlenecks and subsequent limited population sizes in species approaching extinction. Previous genetic studies have highlighted questions about how the Holocene Wrangel population was established and how the isolation event affected genetic diversity. Here, we generated high‐quality mitogenomes from 21 radiocarbon‐dated woolly mammoths to compare the ancestral large and genetically diverse Late Pleistocene Siberian population and the small Holocene Wrangel population. Our results indicate that mitogenome diversity was reduced to one single haplotype at the time of the isolation, and thus that the Holocene Wrangel Island population was established by a single maternal lineage. Moreover, we show that the ensuing small effective population size coincided with fixation of a nonsynonymous mutation, and a comparative analysis of mutation rates suggests that the evolutionary rate was accelerated in the Holocene population. These results suggest that isolation on Wrangel Island led to an increase in the frequency of deleterious genetic variation, and thus are consistent with the hypothesis that strong genetic drift in small populations leads to purifying selection being less effective in removing deleterious mutations.

Effects of water pollution and river fragmentation on population genetic structure of invasive mosquitofish

We analyzed variation at the GPI-2 locus and eleven microsatellite loci of eastern mosquitofish Gambusia holbrooki populations introduced to the Ebro River (Spain), sampling above and below a dam (Flix Reservoir) where severe chronic pollution has been well documented. Allele frequency changes at the GPI-2 locus in the sites nearest to the polluted sediments agree with previous results from studies in mercury-exposed populations of this highly invasive fish. Genetic distinction of the mosquitofish collected close to the polluted sediments was detected at the GPI locus but also at the presumptive neutral microsatellite loci. Recent migration rates estimated from microsatellites indicated that around 30% of fish collected in a specific location were immigrants from upstream and downstream sources. Such high migration rates probably contribute to the mosquitofishs invasive success and suggest that the consequences on the mosquitofish regional genetic structured of high levels of water toxicants could be mediated by immigration from other sites, but the effect of pollutants on local diversity might be higher than observed here.