Dataset Information

Pleiotropy facilitates local adaptation to distant optima in common ragweed (Ambrosia artemisiifolia).

ABSTRACT: Pleiotropy, the control of multiple phenotypes by a single locus, is expected to slow the rate of adaptation by increasing the chance that beneficial alleles also have deleterious effects. However, a prediction arising from classical theory of quantitative trait evolution states that pleiotropic alleles may have a selective advantage when phenotypes are distant from their selective optima. We examine the role of pleiotropy in regulating adaptive differentiation among populations of common ragweed (Ambrosia artemisiifolia); a species that has recently expanded its North American range due to human-mediated habitat change. We employ a phenotype-free approach by using connectivity in gene networks as a proxy for pleiotropy. First, we identify loci bearing footprints of local adaptation, and then use genotype-expression mapping and co-expression networks to infer the connectivity of the genes. Our results indicate that the putatively adaptive loci are highly pleiotropic, as they are more likely than expected to affect the expression of other genes, and they reside in central positions within the gene networks. We propose that the conditionally advantageous alleles at these loci avoid the cost of pleiotropy by having large phenotypic effects that are beneficial when populations are far from their selective optima. We further use evolutionary simulations to show that these patterns are in agreement with a model where populations face novel selective pressures, as expected during a range expansion. Overall, our results suggest that highly connected genes may be targets of positive selection during environmental change, even though they likely experience strong purifying selection in stable selective environments.

SUBMITTER: Hamala T

PROVIDER: S-EPMC7135370 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Pleiotropy facilitates local adaptation to distant optima in common ragweed (Ambrosia artemisiifolia).

Hämälä Tuomas T Gorton Amanda J AJ Moeller David A DA Tiffin Peter P

PLoS genetics 20200325 3

Pleiotropy, the control of multiple phenotypes by a single locus, is expected to slow the rate of adaptation by increasing the chance that beneficial alleles also have deleterious effects. However, a prediction arising from classical theory of quantitative trait evolution states that pleiotropic alleles may have a selective advantage when phenotypes are distant from their selective optima. We examine the role of pleiotropy in regulating adaptive differentiation among populations of common ragwee ...[more]

PMID: 32210431

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Project description:BACKGROUND: Ambrosia artemisiifolia is a North American native that has become one of the most problematic invasive plants in Europe and Asia. We studied its worldwide population genetic structure, using both nuclear and chloroplast microsatellite markers and an unprecedented large population sampling. Our goals were (i) to identify the sources of the invasive populations; (ii) to assess whether all invasive populations were founded by multiple introductions, as previously found in France; (iii) to examine how the introductions have affected the amount and structure of genetic variation in Europe; (iv) to document how the colonization of Europe proceeded; (v) to check whether populations exhibit significant heterozygote deficiencies, as previously observed. PRINCIPAL FINDINGS: We found evidence for multiple introductions of A. artemisiifolia, within regions but also within populations in most parts of its invasive range, leading to high levels of diversity. In Europe, introductions probably stem from two different regions of the native area: populations established in Central Europe appear to have originated from eastern North America, and Eastern European populations from more western North America. This may result from differential commercial exchanges between these geographic regions. Our results indicate that the expansion in Europe mostly occurred through long-distance dispersal, explaining the absence of isolation by distance and the weak influence of geography on the genetic structure in this area in contrast to the native range. Last, we detected significant heterozygote deficiencies in most populations. This may be explained by partial selfing, biparental inbreeding and/or a Wahlund effect and further investigation is warranted. CONCLUSIONS: This insight into the sources and pathways of common ragweed expansion may help to better understand its invasion success and provides baseline data for future studies on the evolutionary processes involved during range expansion in novel environments.

Project description:Climate change is affecting the growth, phenology, and distribution of species across northeastern United States. In response to these changes, some species have been adversely impacted while others have benefited. One species that has benefited from climate change, historically and in response to experimental treatments, is common ragweed (Ambrosia artemisiifolia), a widely distributed annual weed and a leading cause of hay fever in North America. To better understand how climate change may affect the distribution of common ragweed, we built a maximum entropy (Maxent) predictive model using climate and bioclimatic data and over 700 observations across the eastern U.S. Our model performed well with an AUC score of 0.765 using four uncorrelated variables, including precipitation seasonality, mean diurnal temperature range, August precipitation, and January maximum temperature. After building and testing our model, we then projected potential future common ragweed distribution using a suite of 13 global climate models (GCMs) under two future greenhouse gas scenarios for mid and late-century. In addition to providing georeferenced hot spots of potential future expansion, we also provide a metric of confidence by evaluating the number of GCMs that agree. We show a substantial contraction of common ragweed in central Florida, southern Appalachian Mountains, and northeastern Virginia and areas of potential expansion at the northern margins of its current distribution, notably in northeastern U.S. However, the vast majority of this increase is projected to occur by mid-century and may be moderated somewhat by the 2070s, implying that common ragweed may be sensitive to climatic variability. Although other factors and modeling approaches should be explored, we offer preliminary insight into where common ragweed might be a new concern in the future. Due to the health impacts of ragweed, local weed control boards may be well advised to monitor areas of expansion and potentially increase eradication efforts.

Project description:Ragweed allergy is a major public health concern. Within Europe, ragweed is an introduced species and research has indicated that the amounts of ragweed pollen are likely to increase over Europe due to climate change, with corresponding increases in ragweed allergy. To address this threat, improving our understanding of predisposing factors for allergic sensitisation to ragweed and disease is necessary, specifically focusing upon factors that are potentially modifiable (i.e., environmental). In this study, a total of 4013 children aged 2?13 years were recruited across Croatia to undergo skin prick tests to determine sensitisation to ragweed and other aeroallergens. A parental questionnaire collected home environment, lifestyle, family and personal medical history, and socioeconomic information. Environmental variables were obtained using Geographical Information Systems and data from nearby pollen, weather, and air pollution stations. Logistic regression was performed (clustered on school) focusing on risk factors for allergic sensitisation and disease. Ragweed sensitisation was strongly associated with ragweed pollen at levels over 5000 grains m?3 year−1 and, above these levels, the risk of sensitisation was 12?16 times greater than in low pollen areas with about 400 grains m?3 year−1. Genetic factors were strongly associated with sensitisation but nearly all potentially modifiable factors were insignificant. This included measures of local land use and proximity to potential sources of ragweed pollen. Rural residence was protective (odds ratio (OR) 0.73, 95% confidence interval (CI) 0.55?0.98), but the factors underlying this association were unclear. Being sensitised to ragweed doubled (OR 2.17, 95% CI 1.59?2.96) the risk of rhinoconjunctivitis. No other potentially modifiable risk factors were associated with rhinoconjunctivitis. Ragweed sensitisation was strongly associated with ragweed pollen, and sensitisation was significantly associated with rhinoconjunctivitis. Apart from ragweed pollen levels, few other potentially modifiable factors were significantly associated with ragweed sensitisation. Hence, strategies to lower the risk of sensitisation should focus upon ragweed control.

Dataset Information

Pleiotropy facilitates local adaptation to distant optima in common ragweed (Ambrosia artemisiifolia).

Publications

Pleiotropy facilitates local adaptation to distant optima in common ragweed (Ambrosia artemisiifolia).

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