Recent evidence demonstrates that novel protein-coding genes can arise de novo from nongenic loci. This evolutionary innovation is thought to be facilitated by the pervasive translation of non-genic transcripts, which exposes a reservoir of variable polypeptides to natural selection. Here, we systematically characterize how these de novo emerging coding sequences impact fitness in budding yeast. Disruption of emerging sequences is generally inconsequential for fitness in the laboratory and in natural populations. Overexpression of emerging sequences, however, is enriched in adaptive fitness effects compared to overexpression of established genes. We find that adaptive emerging sequences tend to encode putative transmembrane domains, and that thymine-rich intergenic regions harbor a widespread potential to produce transmembrane domains. These findings, together with in-depth examination of the de novo emerging YBR196C-A locus, suggest a novel evolutionary model whereby adaptive transmembrane polypeptides emerge de novo from thymine-rich nongenic regions and subsequently accumulate changes molded by natural selection.
Ocean currents are expected to be the predominant environmental factor influencing the dispersal of planktonic larvae or spores; yet, their characterization as predictors of marine connectivity has been hindered by a lack of understanding of how best to use oceanographic data. We used a high-resolution oceanographic model output and Lagrangian particle simulations to derive oceanographic distances (hereafter called transport times) between sites studied for Macrocystis pyrifera genetic differentiation. We build upon the classical isolation-by-distance regression model by asking how much additional variability in genetic differentiation is explained when adding transport time as predictor. We explored the extent to which gene flow is dependent upon seasonal changes in ocean circulation. Because oceanographic transport between two sites is inherently asymmetric, we also compare the explanatory power of models using the minimum or the mean transport times. Finally, we compare the direction of connectivity as estimated by the oceanographic model and genetic assignment tests. We show that the minimum transport time had higher explanatory power than the mean transport time, revealing the importance of considering asymmetry in ocean currents when modelling gene flow. Genetic assignment tests were much less effective in determining asymmetry in gene flow. Summer-derived transport times, in particular for the month of June, which had the strongest current speed, greatest asymmetry and highest spore production, resulted in the best-fit model explaining twice the variability in genetic differentiation relative to models that use geographic distance or habitat continuity. The best overall model also included habitat continuity and explained 65% of the variation in genetic differentiation among sites.
Aim Past climate-driven range shifts shaped intraspecific diversities of species world-wide. Earlier studies, focused on glacial refugia, might have overlooked genetic erosion at lower latitudes associated with warmer periods. For marine species able to colonize deeper waters, depth shifts might be important for local persistence, preventing some latitudinal shifts, analogous to elevational refugia in terrestrial habitats. In this study, we asked whether past latitudinal or depth range shifts explain extant gene pools in Saccorhiza polyschides, a large habitat structuring brown alga distributed from coastal to offshore deep reefs.Location North-east Atlantic and western Mediterranean basin.Methods Genetic structure and diversity were inferred using seven microsatellite loci, for 27 sites throughout the entire distributional range. Ecological niche modelling (ENM) was performed with and without information about genetic structure (sub-taxon niche structure) to predict distributions for the Last Glacial Maximum (LGM), the warmer Mid-Holocene (MH) and the present.Results Both ENM approaches predicted a wider potential distribution in deeper waters than is presently known, a post-glacial expansion to northern shores and the extirpation of southern edges during the warmer MH. Genetic data corroborated range dynamics, revealing three major genetic groups with current boundaries in the Bay of Biscay and the Lisbon coastal region, pinpointing ancient refugial origins. Despite extensive southern range contraction, the southernmost warmer regions are still the richest in genetic diversity, indicating long-term persistence of large populations. ENMs suggested that this could only have been possible due to stable refugia in deeper reefs. Main conclusionsThe global distribution of gene pools of temperate marine forests is explained by past range shifts that structured both latitudinal glacial refugia and depth refugia during warmer periods. Deep rear edge populations play a fundamental role during periods of extreme climate, allowing persistence and retaining some of the largest genetic diversity pools of the species' distribution.
Aim Drivers of intraspecific biodiversity include past climate‐driven range shifts and contemporary ecological conditions mediating connectivity, but these are rarely integrated in a common comprehensive approach. This is particularly relevant for marine organisms, as ocean currents strongly influence population isolation or connectivity, keeping or diluting the signatures left by past climates. Here we ask whether the coupling between past range shifts and contemporary connectivity explain the extant gene pools of Laminaria ochroleuca, a large brown alga structuring important marine forests from shallow to deep infralittoral grounds. Location Northeastern Atlantic Ocean. Taxon Laminaria ochroleuca. Methods We estimated population genetic diversity and structure of L. ochroleuca across its entire distribution range using 15 polymorphic microsatellite markers. This was compared with the outcomes of a palaeoclimatic model predicting latitudinal and depth range shifts from the Last Glacial Maximum (LGM) to the present. Genetic differentiation was further compared with potential connectivity inferred with a biophysical model developed with high‐resolution data from HYCOM (Hybrid Coordinate Ocean Model). Results The biogeographical distribution of genetic variability showed overall agreement with the predictions from independently inferred past range shifts. Multiple regions of persistence were identified in deep and upwelling settings at the lowest latitudes of the current species distribution, where higher and unique genetic diversity was retained. The biophysical model revealed that despite the possibility of long‐distance migration, contemporary oceanographic barriers strongly restrict connectivity of isolated genetic lineages. Main conclusions Integrating different processes at biogeographical scales explained the extant gene pools of marine forests of L. ochroleuca. Low‐latitude genetic relics harbour a disproportional evolutionary significance, persisting as ancient populations in isolated deep and upwelling climate refugia. Their inferred rates of dispersal may be insufficient to accommodate anticipated climate warming.
Abstract. Isolation by distance (IBD) models are widely used to predict levels of genetic connectivity as a function of Euclidean distance, and although recent studies have used GISlandscape ecological approaches to improve the predictability of spatial genetic structure, few if any have addressed the effect of habitat continuity on gene flow. Landscape effects on genetic connectivity are even less understood in marine populations, where habitat mapping is particularly challenging. In this study, we model spatial genetic structure of a habitatstructuring species, the giant kelp Macrocystis pyrifera, using highly variable microsatellite markers. GIS mapping was used to characterize habitat continuity and distance between sampling sites along the mainland coast of the Santa Barbara Channel, and their roles as predictors of genetic differentiation were evaluated. Mean dispersal distance (r) and effective population size (N e ) were estimated by comparing our IBD slope with those from simulations incorporating habitat continuity and spore dispersal characteristics of the study area. We found an allelic richness of 7-50 alleles/locus, which to our knowledge is the highest reported for macroalgae. The best regression model relating genetic distance to habitat variables included both geographic distance and habitat continuity, which were respectively, positively and negatively related to genetic distance. Our results provide strong support for a dependence of gene flow on both distance and habitat continuity and elucidate the combination of N e and r that explained genetic differentiation.
The genetic consequences of living on the edge of distributional ranges have been the subject of a largely unresolved debate. Populations occurring along persistent low latitude ranges (rear-edge) are expected to retain high and unique genetic diversity. In contrast, currently less favourable environmental conditions limiting population size at such range-edges may have caused genetic erosion that prevails over past historical effects, with potential consequences on reducing future adaptive capacity. The present study provides an empirical test of whether population declines towards a peripheral range might be reflected on decreasing diversity and increasing population isolation and differentiation. We compare population genetic differentiation and diversity with trends in abundance along a latitudinal gradient towards the peripheral distribution range of Saccorhiza polyschides , a large brown seaweed that is the main structural species of kelp forests in SW Europe. Signatures of recent bottleneck events were also evaluated to determine whether the recently recorded distributional shifts had a negative influence on effective population size. Our findings show decreasing population density and increasing spatial fragmentation and local extinctions towards the southern edge. Genetic data revealed two well supported groups with a central contact zone. As predicted, higher differentiation and signs of bottlenecks were found at the southern edge region. However, a decrease in genetic diversity associated with this pattern was not verified. Surprisingly, genetic diversity increased towards the edge despite bottlenecks and much lower densities, suggesting that extinctions and recolonizations have not strongly reduced diversity or that diversity might have been even higher there in the past, a process of shifting genetic baselines.
At small spatial and temporal scales, genetic differentiation is largely controlled by constraints on gene flow, while genetic diversity across a species' distribution is shaped on longer temporal and spatial scales. We assess the hypothesis that oceanographic transport and other seascape features explain different scales of genetic structure of giant kelp, Macrocystis pyrifera. We followed a hierarchical approach to perform a microsatellite-based analysis of genetic differentiation in Macrocystis across its distribution in the northeast Pacific. We used seascape genetic approaches to identify large-scale biogeographic population clusters and investigate whether they could be explained by oceanographic transport and other environmental drivers. We then modelled population genetic differentiation within clusters as a function of oceanographic transport and other environmental factors. Five geographic clusters were identified: Alaska/Canada, central California, continental Santa Barbara, California Channel Islands and mainland southern California/Baja California peninsula. The strongest break occurred between central and southern California, with mainland Santa Barbara sites forming a transition zone between the two. Breaks between clusters corresponded approximately to previously identified biogeographic breaks, but were not solely explained by oceanographic transport. An isolation-by-environment (IBE) pattern was observed where the northern and southern Channel Islands clustered together, but not with closer mainland sites, despite the greater distance between them. The strongest environmental association with this IBE pattern was observed with light extinction coefficient, which extends suitable habitat to deeper areas. Within clusters, we found support for previous results showing that oceanographic connectivity plays an important role in the population genetic structure of Macrocystis in the Northern hemisphere.
The global redistribution of biodiversity will intensify in the coming decades of climate change, making projections of species range shifts and of associated genetic losses important components of conservation planning. Highly-structured marine species, notably brown seaweeds, often harbor unique genetic variation at warmer low-latitude rear edges and thus are of particular concern. Here, a combination of Ecological Niche Models (ENMs) and molecular data is used to forecast the potential near-future impacts of climate change for a warm-temperate, canopy forming seaweed, Bifurcaria bifurcata. ENMs for B. bifurcata were developed using marine and terrestrial climatic variables, and its range projected for 2040-50 and 2090-2100 under two greenhouse emission scenarios. Geographical patterns of genetic diversity were assessed by screening 18 populations spawning the entire distribution for two organelle genes and 6 microsatellite markers. The southern limit of B. bifurcata was predicted to shift northwards to central Morocco by the mid-century. By 2090-2100, depending on the emission scenario, it could either retreat further north to western Iberia or be relocated back to Western Sahara. At the opposing margin, B. bifurcata was predicted to expand its range to Scotland or even Norway. Microsatellite diversity and endemism were highest in Morocco, where a unique and very restricted lineage was also identified. Our results imply that B. bifurcata will maintain a relatively broad latitudinal distribution. Although its persistence is not threatened, the predicted extirpation of a unique southern lineage or even the entire Moroccan diversity hotspot will erase a rich evolutionary legacy and shrink global diversity to current (low) European levels. NW Africa and similarly understudied southern regions should receive added attention if expected range changes and diversity loss of warm-temperate species is not to occur unnoticed.
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