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.

QTL analysis reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

“…Pleiotropic effects of flowering time genes on growth have been frequently identified (Auge et al, 2019). This evidence of co-localised height and flowering time QTL also lends support to a recent study on common ragweed, which (by proxy measurement) discovered that widespread pleiotropy facilitates local adaptation in this species, particularly when populations were far from their selective optima (Hämälä, Gorton, Moeller, & Tiffin, 2020).…”

Pleiotropy facilitates parallel adaptation in sticklebacks

“…These recent findings conflict with earlier theoretical work suggesting that pleiotropy is constraining and should always be disfavoured (Fisher, 1930;Orr, 2000;Otto, 2004). Our results are also contrary to the suggestion that genes and mutations that minimize pleiotropy will contribute more often to repeated phenotypic evolution (Martin & Orgogozo, 2013;Stern & Orgogozo, 2008), but consistent with more recent work demonstrating that pleiotropic loci can contribute to adaptive phenotypic evolution (Archambeault et al, 2020;Greenwood et al, 2016;Hämälä et al, 2020;Lewis et al, 2019;Mills et al, 2014;Nagy et al, 2018;Smith, 2016).…”

“…However, it is important to note that the data was from European stream‐lake populations, which are very distantly related to the Canadian stream‐lake populations used here and exhibit very little genetic parallelism (Rennison et al, 2020 ). Despite the different biases and limitations of these two metrics, when taken together they provide complementary (i.e., phenotype‐dependent and phenotype‐independent) estimates of pleiotropy (Hämälä et al, 2020 ).…”

“…Network connectivity can indicate gene regulatory interactions, protein‐protein interactions, or position in metabolic pathways (Proulx et al, 2005 ). Furthermore, gene connectivity has been found to be an important determinant of evolutionary constraint when responding to a selective challenge; genes with higher levels of connectivity tend to evolve at a slower rate (Mähler et al, 2017 ; Masalia et al, 2017 ) and are associated with signatures of local adaptation (Hämälä et al, 2020 ). By using two different proxies, we were able to evaluate whether the observed relationship between genomic parallelism and pleiotropy was robust to the metric used.…”

Population genomics of parallel adaptation

“…Beyond its impact on hay‐fever (allergy) and asthma sufferers, ragweed is an important agricultural weed, especially in the invaded range, and appears to have also adapted to urban environments in the USA (Gorton et al., 2018). The broad spectrum of tools in modern ecological genetics—crossing designs (McGoey et al., 2017), quantitative genetics (McGoey and Stinchcombe, 2018), manipulative experiments in the field (Gorton et al., 2019; Sun et al., 2020), genotyping by sequencing and population genetics (Martin et al., 2016; van Booheemen et al, 2017, 2018; van Boheemen & Hodgins, 2020; McGoey et al., 2020), transcriptomics (Hämälä et al., 2020)—is available in an annual plant that is of agricultural and health importance (Montagnani et al., 2017), and with a rich history of ecological investigation (e.g. MacDonald & Kotanen, 2010).…”