Drought-induced trans-generational tradeoff between stress tolerance and defence: consequences for range limits?

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Most transplant experiments across species geographic range boundaries indicate that adaptation to stressful environments outside the range is often constrained. However, the mechanisms of these constraints remain poorly understood. We used extended generation crosses from diverged high and low elevation populations. In experiments across low elevation range boundaries, there was selection on the parental lines for abiotic stress‐tolerance and resistance to herbivores. However, in support of a defense‐tolerance trade‐off, extended generation crosses showed nonindependent segregation of these traits in the laboratory across a drought‐stress gradient and in the field across the low elevation range boundary. Genotypic variation in a marker from a region of the genome containing a candidate gene (MYC2) was associated with change in the genetic trade‐off. Thus, using crosses and forward genetics, we found experimental genetic and molecular evidence for a pleiotropic trade‐off that could constrain the evolution of range expansion.

Section: Discussionsupporting

confidence: 91%

Section: Methodsmentioning

confidence: 99%

Evolutionary constraint on low elevation range expansion: Defense‐abiotic stress‐tolerance trade‐off in crosses of the ecological model Boechera stricta

Olsen

Gill

Haugen

et al. 2019

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“…These adaptive phenotypes may be expressed constitutively or may be induced by an environmental cue that predicts a change in water availability later in the life of the organism. Increasingly, experimental studies show that the parental soil moisture regime can also adaptively influence the development of progeny (Alsdurf, Anderson, & Siemens, ; Alsdurf, Ripley, Matzner, & Siemens, ), providing a third route by which plants can fine tune the phenotypes of their offspring to local soil moisture levels. For instance, in Massachusetts genotypes of the annual plant Polygonum persicaria , offspring of drought‐stressed parents make more extensive root systems and deploy them faster in response to drought as compared to offspring of well‐watered parents.…”

Section: Discussionmentioning

confidence: 99%

Empirical patterns of environmental variation favor adaptive transgenerational plasticity

Colicchio

Herman

2020

Effects of parental environment on offspring traits have been well known for decades. Interest in this transgenerational form of phenotypic plasticity has recently surged due to advances in our understanding of its mechanistic basis. Theoretical research has simultaneously advanced by predicting the environmental conditions that should favor the adaptive evolution of transgenerational plasticity. Yet whether such conditions actually exist in nature remains largely unexplored. Here, using long‐term climate data, we modeled optimal levels of transgenerational plasticity for an organism with a one‐year life cycle at a spatial resolution of 4 km2 across the continental United States. Both annual temperature and precipitation levels were often autocorrelated, but the strength and direction of these autocorrelations varied considerably even among nearby sites. When present, such environmental autocorrelations render offspring environments statistically predictable based on the parental environment, a key condition for the adaptive evolution of transgenerational plasticity. Results of our optimality models were consistent with this prediction: High levels of transgenerational plasticity were favored at sites with strong environmental autocorrelations, and little‐to‐no transgenerational plasticity was favored at sites with weak or nonexistent autocorrelations. These results are among the first to show that natural patterns of environmental variation favor the evolution of adaptive transgenerational plasticity. Furthermore, these findings suggest that transgenerational plasticity is likely variable in nature, depending on site‐specific patterns of environmental variation.

“…Further, maternal effects may be adaptive so that they enhance offspring fitness in conditions similar to those experienced by the parents (Galloway & Etterson, 2007). Drought experienced by parents has been found to enhance drought tolerance of offspring in B. stricta (Alsdurf, Ripley, Matzner, & Siemens, 2013), but the general importance of maternal effects to trait variation in this species is not known. While we cannot rule out potential transgenerational effects on the observed phenotypic variation, it is likely that the seeds used in the experiment ma- One factor that may play a role in the maintenance of multiple phenotypically distinct lineages in a population is environmental heterogeneity on a local scale (Gillespie & Turelli, 1989;Linhart & Grant, 1996;Salmela, 2014).…”

Section: Discussionmentioning

confidence: 99%

Natural quantitative genetic variance in plant growth differs in response to ecologically relevant temperature heterogeneity

Salmela

Ewers

Weinig

2016

Adaptation to large‐scale spatial heterogeneity in the environment accounts for a major proportion of genetic diversity within species. Theory predicts the erosion of adaptive genetic variation on a within‐population level, but considerable genetic diversity is often found locally. Genetic diversity could be expected to be maintained within populations in temporally or spatially variable conditions if genotypic rank orders vary across contrasting microenvironmental settings. Taking advantage of fine‐resolution environmental data, we tested the hypothesis that temperature heterogeneity among years could be one factor maintaining quantitative genetic diversity within a natural and genetically diverse plant population. We sampled maternal families of Boechera stricta, an Arabidopsis thaliana relative, at one location in the central Rocky Mountains and grew them in three treatments that, based on records from an adjacent weather station, simulated hourly temperature changes at the native site during three summers with differing mean temperatures. Treatment had a significant effect on all traits, with 2–3‐fold increase in above‐ and belowground biomass and the highest allocation to roots observed in the treatment simulating the warmest summer on record at the site. Treatment affected bivariate associations between traits, with the weakest correlation between above‐ and belowground biomass in the warmest treatment. The magnitude of quantitative genetic variation for all traits differed across treatments: Genetic variance of biomass was 0 in the warmest treatment, while highly significant diversity was found in average conditions, resulting in broad‐sense heritability of 0.31. Significant genotype × environment interactions across all treatments were found only in root‐to‐shoot ratio. Therefore, temperature variation among summers appears unlikely to account for the observed levels of local genetic variation in size in this perennial species, but may influence family rank order in growth allocation. Our results indicate that natural environmental fluctuations can have a large impact on the magnitude of within‐population quantitative genetic variance.