Epigenetic Inheritance across the Landscape

The study of epigenomic variation at the landscape-level in plants may add important insight to studies of adaptive variation. A major goal of landscape genomic studies is to identify genomic regions contributing to adaptive variation across the landscape. Heritable variation in epigenetic marks, resulting in transgenerational plasticity, can influence fitness-related traits. Epigenetic marks are influenced by the genome, the environment, and their interaction, and can be inherited independently of the genome. Thus, epigenomic variation likely influences the heritability of many adaptive traits, but the extent of this influence remains largely unknown. Here we summarize the relevance of epigenetic inheritance to ecological and evolutionary processes, and review the literature on landscape-level patterns of epigenetic variation. Landscape-level patterns of epigenomic variation in plants generally show greater levels of isolation by distance and isolation by environment then is found for the genome, but the causes of these patterns are not yet clear. Linkage between the environment and epigenomic variation has been clearly shown within a single generation, but demonstrating transgenerational inheritance requires more complex breeding and/or experimental designs. Transgenerational epigenetic variation may alter the interpretation of landscape genomic studies that rely upon phenotypic analyses, but should have less influence on landscape genomic approaches that rely upon outlier analyses or genome-environment associations. We suggest that multi-generation common garden experiments conducted across multiple environments will allow researchers to understand which parts of the epigenome are inherited, as well as to parse out the relative contribution of heritable epigenetic variation to the phenotype

Optimal defense theory explains deviations from latitudinal herbivory defense hypothesis

The latitudinal herbivory defense hypothesis (LHDH) postulates that the prevalence of species interactions, including herbivory, is greater at lower latitudes, leading to selection for increased levels of plant defense. While latitudinal defense clines may be caused by spatial variation in herbivore pressure, optimal defense theory predicts that clines could also be caused by ecogeographic variation in the cost of defense. For instance, allocation of resources to defense may not increase plant fitness when growing seasons are short and plants must reproduce quickly. Here we use a common garden experiment to survey genetic variation for constitutive and induced phenylpropanoid glycoside (PPG) concentrations across 35 Mimulus guttatus populations over a similar to 13 degrees latitudinal transect. Our sampling regime is unique among studies of the LHDH in that it allows us to disentangle the effects of growing season length from those of latitude, temperature, and elevation. For five of the seven PPGs surveyed, we find associations between latitude and plant defense that are robust to population structure. However, contrary to the LHDH, only two PPGs were found at higher levels in low latitude populations, and total PPG concentrations were higher at higher latitudes. PPG levels are strongly correlated with growing season length, with higher levels of PPGs in plants from areas with longer growing seasons. Further, flowering time is positively correlated with the concentration of nearly all PPGs, suggesting that there may be a strong trade--off between development time and defense production. Our results reveal that ecogeographic patterns in plant defense may reflect variation in the cost of producing defense compounds in addition to variation in herbivore pressure. Thus, the biogeographic pattern predicted by the LHDH may not be accurate because the underlying factors driving variation in defense, in this case, growing season length, are not always associated with latitude in the same manner. Given these results, we conclude that LHDH cannot be interpreted without considering life history, and we recommend that future work on the LHDH move beyond solely testing the core LHDH prediction and place greater emphasis on isolating agents of selection that generate spatial variation in defense and herbivore pressure.NSF [IOS-1558035]; Northern Arizona University; University of Virginia; University of California, Berkeley12 month embargo; first published: 10 January 2017.This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

The genetic correlation between flower size and water use efficiency in monkeyflowers

This is the publisher's version, also available electronically from http://www.evolutionary-ecology.com/.Question: Does water loss during drought stress represent an important physiological constraint on the evolution of flower size? Organism: A genetically diverse population of Mimulus guttatus (yellow monkeyflower) originally sampled from an alpine meadow in Oregon, USA. Methods: We grew plants of three different genotypic classes (small, medium, and large flowered) under both well-watered and drought-stress conditions and measured water use efficiency using stable carbon isotopes. Results: There was no difference in water use efficiency among flower size genotypes under well-watered conditions, but the water use efficiency of small-flowered plants was substantially lower than that of medium or large genotypes under drought stress. Whether this paradoxical result is a direct effect of flower size or an indirect (i.e. pleiotropic) effect, the presence of a genetic correlation between floral and physiological traits indicates that selection of one does impact the other

The Genetics of Phenotypic Plasticity in Plant Defense: Trichome Production in Mimulus guttatus

This is the publisher's version, also available electronically from http://www.jstor.org/stable/10.1086/651300#fn1.Insect herbivory is a major driving force of plant evolution. Phenotypic plasticity and developmental variation provide a means for plants to cope with variable herbivory. We characterized the genetics of developmental variation and phenotypic plasticity in trichome density, a putative defensive trait of Mimulus guttatus (yellow monkeyflower). Our results are evaluated in relation to the optimal defense theory, which provides testable predictions for plastic and developmental patterns in defense traits. We found that both developmental stage and simulated insect damage affected trichome production, but in different ways. Plants were more likely to produce at least some trichomes on later leaves than on earlier leaves, regardless of damage. Damage did not affect the average probability of producing trichomes, but it did increase the density of hairs on trichome‐positive plants. We mapped trichome quantitative trait loci (QTL) by selectively genotyping a large panel of recombinant inbred lines derived from two highly divergent populations. Several highly pleiotropic QTL influenced multiple aspects of the trichome phenotype (constitutive, developmental, and/or plastic responses). Only one of the QTL influenced trichome induction following damage. In a result that is consistent with a central prediction of optimal defense theory, the high allele at this location was from the ancestral population with low constitutive trichome production

A test of the evolution of increased competitive ability in two invaded regions

Non-native plant species invasions can have significant ecological and economic impacts. Finding patterns that predict and explain the success of non-native species has thus been an important focus in invasion ecology. The evolution of increased competitive ability (EICA) hypothesis has been a frequently used framework to understand invasion success. Evolution of increased competitive ability predicts that (1) non-native populations will escape from coevolved specialist herbivores that were present within the native range and this release from specialist herbivores should result in relaxed selection pressure on specialist-related defense traits, (2) there will be a trade-off between allocation of resources for resistance against specialist herbivores and allocation to traits related to competitive ability, and (3) this shift will allow more allocation to competitive ability traits. We tested the predictions of EICA in the model plant Mimulus guttatus, a native of western North America (WNA). We compared how well the predictions of EICA fit patterns in two non-native regions, the United Kingdom (UK), an older more successful invasion, and eastern North America (ENA), a younger less successful invasion. We completed extensive herbivore surveys and grew plants derived from multiple populations in each region in a common greenhouse environment to test adherence to the predictions of EICA. We found evidence of specialist herbivore escape in the UK, but not the ENA plants. Compared to native plants the UK plants had lower levels of resistance traits, were taller, and produced larger and more flowers, while the ENA plants had mostly equivalent traits to the WNA plants. Plants from the UK conformed to the predictions of EICA more closely than those from ENA. The UK invasion is an older, more successful invasion, suggesting that support for EICA predictions may be highest in more successful invasions

A High-Resolution Genetic Map of Yellow Monkeyflower Identifies Chemical Defense QTLs and Recombination Rate Variation

Genotyping-by-sequencing methods have vastly improved the resolution and accuracy of genetic linkage maps by increasing both the number of marker loci as well as the number of individuals genotyped at these loci. Using restriction-associated DNA sequencing, we construct a dense linkage map for a panel of recombinant inbred lines derived from a cross between divergent ecotypes of Mimulus guttatus. We used this map to estimate recombination rate across the genome and to identify quantitative trait loci for the production of several secondary compounds (PPGs) of the phenylpropanoid pathway implicated in defense against herbivores. Levels of different PPGs are correlated across recombinant inbred lines suggesting joint regulation of the phenylpropanoid pathway. However, the three quantitative trait loci identified in this study each act on a distinct PPG. Finally, we map three putative genomic inversions differentiating the two parental populations, including a previously characterized inversion that contributes to life-history differences between the annual/perennial ecotypes.We thank M. Montenero and K. Keefover-Ring for assistance in phytochemistry sample preparation and HPLC troubleshooting, respectively. The KU EEB Genetics group provided valuable comments on the manuscript. We also thank Emma Huang and two anonymous reviewers for their comments. Funding for this research was provided by National Science Foundation grants DEB-0841609 (to RLL) and IOS-0951254 (to J.K.K.), by NIH grant GM073990 (to J.K.K.), and funding from the University of Kansas Botany Endowment Funds (to P.J.M.)

The case for the continued use of the genus name Mimulus for all monkeyflowers

The genus Mimulus is a well-studied group of plant species, which has for decades allowed researchers to address a wide array of fundamental questions in biology (Wu & al. 2008; Twyford & al. 2015). Linnaeus named the type species of Mimulus (ringens L.), while Darwin (1876) used Mimulus (luteus L.) to answer key research questions. The incredible phenotypic diversity of this group has made it the focus of ecological and evolutionary study since the mid-20th century, initiated by the influential work of Clausen, Keck, and Hiesey as well as their students and collaborators (Clausen & Hiesey 1958; Hiesey & al. 1971, Vickery 1952, 1978). Research has continued on this group of diverse taxa throughout the 20th and into the 21st century (Bradshaw & al. 1995; Schemske & Bradshaw 1999; Wu & al. 2008; Twyford & al. 2015; Yuan 2019), and Mimulus guttatus was one of the first non-model plants to be selected for full genome sequencing (Hellsten & al. 2013). Mimulus has played a key role in advancing our general understanding of the evolution of pollinator shifts (Bradshaw & Schemske 2003; Cooley & al. 2011; Byers & al. 2014), adaptation (Lowry & Willis 2010; Kooyers & al. 2015; Peterson & al. 2016; Ferris & Willis 2018; Troth & al. 2018), speciation (Ramsey & al. 2003; Wright & al. 2013; Sobel & Streisfeld 2015; Zuellig & Sweigart 2018), meiotic drive (Fishman & Saunders 2008), polyploidy (Vallejo-Marín 2012; Vallejo-Marín & al. 2015), range limits (Angert 2009; Sexton et al. 2011; Grossenbacher & al. 2014; Sheth & Angert 2014), circadian rhythms (Greenham & al. 2017), genetic recombination (Hellsten & al. 2013), mating systems (Fenster & Ritland 1994; Dudash & Carr 1998; Brandvain & al. 2014) and developmental biology (Moody & al. 1999; Baker & al. 2011, 2012; Yuan 2019). This combination of a rich history of study coupled with sustained modern research activity is unparalleled among angiosperms. Across many interested parties, the name Mimulus therefore takes on tremendous biological significance and is recognizable not only by botanists, but also by zoologists, horticulturalists, naturalists, and members of the biomedical community. Names associated with a taxonomic group of this prominence should have substantial inertia, and disruptive name changes should be avoided. As members of the Mimulus community, we advocate retaining the genus name Mimulus to describe all monkeyflowers. This is despite recent nomenclature changes that have led to a renaming of most monkeyflower species to other genera.Additional co-authors: Jannice Friedman, Dena L Grossenbacher, Liza M Holeski, Christopher T Ivey, Kathleen M Kay, Vanessa A Koelling, Nicholas J Kooyers, Courtney J Murren, Christopher D Muir, Thomas C Nelson, Megan L Peterson, Joshua R Puzey, Michael C Rotter, Jeffrey R Seemann, Jason P Sexton, Seema N Sheth, Matthew A Streisfeld, Andrea L Sweigart, Alex D Twyford, John H Willis, Kevin M Wright, Carrie A Wu, Yao-Wu Yua

Quantitative trait evolution in Mimulus guttatus (yellow monkeyflower)

Dissertation (Ph.D.)--University of Kansas, Ecology & Evolutionary Biology, 2007.My dissertation examines several aspects of quantitative trait evolution in Mimulus guttatus. In Chapter 2, I use M. guttatus plants to investigate how response to artificial selection on a trait index differs among replicate populations that differ only in mating system. The results show a divergence in response to selection among mating system types, despite an equivalent selection regime and no direct effect of mating system on fitness. In Chapter 3, I use plants derived from several natural populations to look at geographic differences in genetic and environmental variation in a quantitative trait, trichome density. Constitutive production of trichomes is variable both within and among populations of M. guttatus and there is genetic variation for it both within and among geographically distinct natural populations. Damage on early leaves can induce increased trichome production on later leaves, a plastic response that is likely adaptive. In addition, I show in this chapter that trichome induction can be maternally transmitted by a yet undescribed epigenetic mechanism. There is genetic variation among plants in the capacity for both within and between plant generation induction. In Chapter 4, I examine how trichome density affects plant-insect interactions with an herbivore common to some M. guttatus populations, the meadow spittlebug. While trichomes confer resistance to some forms of herbivory, these experiments show that they do not deter meadow spittlebugs, either in their ability to feed or in their feeding preferences