American Naturalist最新文献

AbstractOrganisms experience environments that vary across both space and time. Such environmental heterogeneity shapes standing genetic variation and may influence species' capacity to adapt to rapid environmental change. However, we know little about the kind of genetic variation that is involved in local adaptation to environmental variability. To address this gap, we sequenced the whole genomes of 140 purple sea urchins (Strongylocentrotus purpuratus) from seven populations that vary in their degree of pH variability. Despite no evidence of global population structure, we found a suite of single-nucleotide polymorphisms (SNPs) tightly correlated with local pH variability (outlier SNPs), which were overrepresented in regions putatively involved in gene regulation (long noncoding RNA and enhancers), supporting the idea that variation in regulatory regions is important for local adaptation to variability. In addition, outliers in genes were found to be (i) enriched for biomineralization and ion homeostasis functions related to low pH response, (ii) less central to the protein-protein interaction network, and (iii) underrepresented among genes highly expressed during early development. Taken together, these results suggest that loci that underlie local adaptation to pH variability in purple sea urchins fall in regions with potentially low pleiotropic effects (based on analyses involving regulatory regions, network centrality, and expression time) involved in low pH response (based on functional enrichment).

AbstractGenetic variation within species is crucial for sessile species to adapt to novel environments when facing dramatic climate changes. However, the debate continues whether standing ancestral variation adaptive to current environmental variability is sufficient to guarantee future suitability. Using wild banana Musa itinerans, we investigated the relative contribution of standing ancestral variation versus new mutations to environmental adaptation and inferred their future fate. On the continental island of Taiwan, local populations immigrated from the Southeast Asian continent during the ice age and have been isolated since then. This allows the classification of genetic variants into standing ancestral variation (polymorphic in Taiwan and the continent) and new mutations (polymorphic only in Taiwan). For temperature-related variables where Taiwan is mainly within the ancestral climatic range, standing ancestral variation had a slightly stronger association than new mutations. New mutations were more important for precipitation-related variables, where northeastern Taiwan had much more winter rainfall than most of continental Southeast Asia. Upon future climate change, new mutations showed higher genetic offset in regions of abrupt transition between allele frequency and local environments, suggesting their greater spatial heterogeneity of future vulnerability.

AbstractRecent experimental evidence demonstrates that shifts in mutational biases-for example, increases in transversion frequency-can change the distribution of fitness effects of mutations (DFE). In particular, reducing or reversing a prevailing bias can increase the probability that a de novo mutation is beneficial. It has also been shown that mutator bacteria are more likely to emerge if the beneficial mutations they generate have a larger effect size than observed in the wild type. Here, we connect these two results, demonstrating that mutator strains that reduce or reverse a prevailing bias have a positively shifted DFE, which in turn can dramatically increase their emergence probability. Since changes in mutation rate and bias are often coupled through the gain and loss of DNA repair enzymes, our results predict that the invasion of mutator strains will be facilitated by shifts in mutation bias that offer improved access to previously undersampled beneficial mutations.

AbstractThe joint distribution of selection coefficients and mutation rates is a key determinant of the genetic architecture of molecular adaptation. Three different distributions are of immediate interest: (1) the "nominal" distribution of possible changes, prior to mutation or selection; (2) the "de novo" distribution of realized mutations; and (3) the "fixed" distribution of selectively established mutations. Here, we formally characterize the relationships between these joint distributions under the strong-selection/weak-mutation (SSWM) regime. The de novo distribution is enriched relative to the nominal distribution for the highest rate mutations, and the fixed distribution is further enriched for the most highly beneficial mutations. Whereas mutation rates and selection coefficients are often assumed to be uncorrelated, we show that even with no correlation in the nominal distribution, the resulting de novo and fixed distributions can have correlations with any combination of signs. Nonetheless, we suggest that natural systems with a finite number of beneficial mutations will frequently have the kind of nominal distribution that induces negative correlations in the fixed distribution. We apply our mathematical framework, along with population simulations, to explore joint distributions of selection coefficients and mutation rates from deep mutational scanning and cancer informatics. Finally, we consider the evolutionary implications of these joint distributions together with two additional joint distributions relevant to parallelism and the rate of adaptation.

AbstractEcological heterogeneity can lead to local adaptation when populations exhibit fitness trade-offs among habitats. However, the degree to which local adaptation is affected by the spatial and temporal scale of environmental variation is poorly understood. A multiyear reciprocal transplant experiment was performed with populations of the annual plant Leptosiphon parviflorus living on adjacent serpentine and nonserpentine soil. Local adaptation over this small geographic scale was observed, but there were differences in the temporal variability of selection across habitats. On serpentine soil, the local population had a consistently large survival advantage, presumably as a result of the temporal stability in selection imposed by soil cation content. In contrast, a fecundity advantage was observed for the sandstone population on its native soil type but only in the two study years with the highest rainfall. A manipulative greenhouse experiment demonstrated that the fitness advantage of the sandstone population in its native soil type depends critically on water availability. The temporal variability in local adaptation driven by variation in precipitation suggests that continued drought conditions have the potential to erode local adaptation in these populations. These results show how different selective factors can influence spatial and temporal patterns of variation in fitness trade-offs.

AbstractAcquired photosynthesis transforms genotypically heterotrophic lineages into autotrophs. Transient acquisitions of eukaryotic chloroplasts may provide key evolutionary insight into the endosymbiosis process-the hypothesized mechanism by which eukaryotic cells obtained new functions via organelle retention. Here, we use an eco-evolutionary model to study the environmental conditions under which chloroplast retention is evolutionarily favorable. We focus on kleptoplastidic lineages-which steal functional chloroplasts from their prey-as hypothetical evolutionary intermediates. Our adaptive dynamics analysis reveals a spectrum of evolutionarily stable strategies ranging from phagotrophy to phototrophy to obligate kleptoplasty. Our model suggests that a low-light niche and weak (or absent) trade-offs between chloroplast retention and overall digestive ability favor the evolution of phototrophy. In contrast, when consumers experience strong trade-offs, obligate kleptoplasty emerges as an evolutionary end point. Therefore, the preevolved trade-offs that underlie an evolving lineage's physiology will likely constrain its evolutionary trajectory.

AbstractPopulation spatial synchrony-the tendency for temporal population fluctuations to be correlated across locations-is common and important to metapopulation stability and persistence. One common cause of spatial synchrony, termed the Moran effect, occurs when populations respond to environmental fluctuations, such as weather, that are correlated over space. Although the degree of spatial synchrony in environmental fluctuations can differ between seasons and different population processes occur in different seasons, the impact on population spatial synchrony is uncertain because prior work has largely assumed that the spatial synchrony of environmental fluctuations and their effect on populations are consistent over annual sampling intervals. We used theoretical models to examine how seasonality in population processes and the spatial synchrony of environmental drivers affect population spatial synchrony. We found that population spatial synchrony can depend not only on the spatial synchrony of environmental drivers but also on the degree to which environmental fluctuations are correlated across seasons, locally, and across space. Moreover, measurements of synchrony from "snapshot" population censuses may not accurately reflect synchrony during other parts of the year. Together, these results show that neglecting seasonality in environmental conditions and population processes is consequential for understanding population spatial synchrony and its driving mechanisms.

AbstractOver the past 50 years, a wealth of testable, often conflicting hypotheses have been generated about the evolution of offspring sex ratio manipulation by mothers. Several of these hypotheses have received support in studies of invertebrates and some vertebrate taxa. However, their success in explaining sex ratios in mammalian taxa-especially in primates-has been mixed. Here, we assess the predictions of four different hypotheses about the evolution of biased offspring sex ratios in the baboons of the Amboseli basin in Kenya: the Trivers-Willard, female rank enhancement, local resource competition, and local resource enhancement hypotheses. Using the largest sample size ever analyzed in a primate population ($n=\mathrm{1,372}$ offspring), we test the predictions of each hypothesis. Overall, we find no support for adaptive biasing of sex ratios. Offspring sex is not consistently related to maternal dominance rank or biased toward the dispersing sex, nor is it predicted by group size, population growth rates, or their interaction with maternal rank. Because our sample size confers power to detect even subtle biases in sex ratio, including modulation by environmental heterogeneity, these results suggest that adaptive biasing of offspring sex does not occur in this population.

AbstractDisentangling different types of selection is a common goal in molecular evolution. Elevated d_N/d_S ratios (the ratio of nonsynonymous to synonymous substitution rates) in focal lineages are often interpreted as signs of positive selection. Paradoxically, relaxed purifying selection can also result in elevated d_N/d_S ratios, but tests to distinguish these two causes are seldomly implemented. Here, we reevaluated seven case studies describing elevated d_N/d_S ratios in animal mitochondrial DNA (mtDNA) and their accompanying hypotheses regarding selection. They included flightless lineages versus flighted lineages in birds, bats, and insects and physiological adaptations in snakes, two groups of electric fishes, and primates. We found that elevated d_N/d_S ratios were often not caused by the predicted mechanism, and we sometimes found strong support for the opposite mechanism. We discuss reasons why energetic hypotheses may be confounded by other selective forces acting on mtDNA and caution against overinterpreting singular molecular signals, including elevated d_N/d_S ratios.