Two reproductive traits show contrasting genetic architectures in Plantago lanceolata

Abstract

In many species, temperature‐sensitive phenotypic plasticity (i.e., an individual's phenotypic response to temperature) displays a positive correlation with latitude, a pattern presumed to reflect local adaptation. This geographical pattern raises two general questions: (a) Do a few large‐effect genes contribute to latitudinal variation in a trait? (b) Is the thermal plasticity of different traits regulated pleiotropically? To address the questions, we crossed individuals of Plantago lanceolata derived from northern and southern European populations. Individuals naturally exhibited high and low thermal plasticity in floral reflectance and flowering time. We grew parents and offspring in controlled cool‐ and warm‐temperature environments, mimicking what plants would encounter in nature. We obtained genetic markers via genotype‐by‐sequencing, produced the first recombination map for this ecologically important nonmodel species, and performed quantitative trait locus (QTL) mapping of thermal plasticity and single‐environment values for both traits. We identified a large‐effect QTL that largely explained the reflectance plasticity differences between northern and southern populations. We identified multiple smaller‐effect QTLs affecting aspects of flowering time, one of which affected flowering time plasticity. The results indicate that the genetic architecture of thermal plasticity in flowering is more complex than for reflectance. One flowering time QTL showed strong cytonuclear interactions under cool temperatures. Reflectance and flowering plasticity QTLs did not colocalize, suggesting little pleiotropic genetic control and freedom for independent trait evolution. Such genetic information about the architecture of plasticity is environmentally important because it informs us about the potential for plasticity to offset negative effects of climate change.

Transgenerational Genetic Effects Help Explain Latitudinal Variation in Seed Mass and Germination Timing in Plantago lanceolata

“…Seed traits can be affected by ( 1) temperatures during the maternal generation, (2) maternal genotype, (3) thermal plasticity of the mother, and (4) maternal genotype by temperature interactions [75,78,84]. The positive association between the maternal control of seed traits and latitude parallels the latitudinal pattern for genetically based maternal thermal plasticity in flower color [93,94,106]. Coupling this maternal thermal plasticity with maternal genetic controls could synergistically enhance offspring establishment in cooler and temporally variable environments, and secondarily provide environmental flexibility when dispersing to a new habitat.…”

“…Photoperiodically controlled flowering occurs under long days. Flowers are protogynous, obligately outcrossing [94,110] and predominately wind-pollinated [93]. Thermal plasticity in flower color is positively correlated with latitude and altitude.…”

“…Our two experiments derive from a QTL experiment, in which Marshall et al (2020) [94] explored the genetic architecture of differences in thermal plasticity in flower color and flowering time between northern and southern European populations. Because we used F1 seeds from this experiment, we summarize aspects of the QTL experiment and refer readers to Marshall et al (2020) [94] and to an earlier experiment describing the latitudinal variation in thermal plasticity in flower color (Lacey et al, 2010 [106], for more details). The northern and southern parents used in the QTL study displayed high and low thermal plasticity, respectively, and represented plasticity extremes found in a sample of 29 European P. lanceolata populations.…”

“…P. lanceolata genetically varies in thermal plasticity of floral color, reflectance, and in flowering time along its latitudinal/altitudinal ranges in Europe [93]. Using seeds from a QTL experiment to explore the genetics of these thermal plasticities [94], we tested the hypothesis that northern and southern populations differ genetically in seed mass and germination timing. Specifically, we asked: (1) Are seed mass and germination timing influenced by transgenerational genetic effects?…”

Multiple modes of selection can influence the role of phenotypic plasticity in species' invasions: Evidence from a manipulative field experiment

“…We define plasticity as the ability of a genotype to modify the phenotype of a trait in response to environmental change. Multiple molecular studies now support the existence of such plasticity genes (e.g., Cho et al, 2017;Corl et al, 2018;Des Marais et al, 2013;Gu et al, 2019;Han et al, 2019;Knies et al, 2009;Marshall et al, 2020;Morris et al, 2014;Nilson & Assmann, 2010).…”