Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment

Дата канвертавання24.04.2016
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Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment
Marc T. J. Johnson1, Anurag A. Agrawal2, John L. Maron3 & Juha-Pekka Salminen4

1Department of Plant Biology, Gardner Hall, North Carolina State University, Raleigh, NC 27695, USA.

2Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, NY 14853, USA (agrawal@cornell.edu)

3Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA (john.maron@mso.umt.edu)

4Department of Chemistry, Laboratory of Organic Chemistry and Chemical Biology, University of Turku, Turku, FI-20014, FINLAND (j-p.salminen@utu.fi)
Running title: Selection on heritable plant traits in the field
Author for correspondence: Marc Johnson, Tel: 919-515-0478, email: marc_johnson@ncsu.edu


This study explored genetic variation and co-variation in multiple functional plant traits. Our goal was to characterize selection, heritibilities and genetic correlations among different types of traits to gain insight into the evolutionary ecology of plant populations and their interactions with insect herbivores. In a field experiment, we detected significant heritable variation for each of 24 traits of Oenothera biennis and extensive genetic covariance among traits. Traits with diverse functions formed several distinct groups that exhibited positive genetic covariation with each other. Genetic variation in life-history traits and secondary chemistry together explained a large proportion of variation in herbivory (r2 = 0.73). At the same time, selection acted on lifetime biomass, life-history traits and two secondary compounds of O. biennis, explaining over 95% of the variation in relative fitness among genotypes. The combination of genetic covariances and directional selection acting on multiple traits suggests that adaptive evolution of particular traits is constrained, and that correlated evolution of groups of traits will occur, which is expected to drive the evolution of increased herbivore susceptibility. As a whole, our study indicates that an examination of genetic variation and covariation among many different types of traits can provide greater insight into the evolutionary ecology of plant populations and plant-herbivores interactions.

Keywords: adaptation; evolvability; G-matrix; genetic variance; heritability; phytochemistry; plant defense; plant function; resistance


An important goal of evolutionary ecology is to understand how functional trait variation influences ecological interactions and adaptation to various environments. For example, ecophysiological traits relating to photosynthesis and plant structure are key adaptations to different abiotic environments (Ackerly, 2004; Hemsley & Poole, 2004). Similarly, variation in life-history traits such as lifespan, phenology and biomass have large impacts on fitness and the success of organisms under different biotic and abiotic conditions (Roff, 1992; Stearns, 1992). Finally, many studies of plant-insect interactions have shown that secondary metabolites are adaptations that provide resistance against herbivory (Dethier, 1941; Berenbaum et al., 1986; Karban & Baldwin, 1997; Agrawal, 2005). Although suites of ecophysiological, life-history, resistance and morphological traits have been studied in isolation, surprisingly few studies have integrated these classes of traits into a comprehensive evolutionary ecological framework. Such an approach could provide greater insight into the ecological and evolutionary significance of genetic variation.

The genetic variation and covariation of traits has several important consequences for studying the evolutionary ecology of plants. First, traits must be heritable for natural selection to result in evolutionary change within populations. Second, genetic covariance among traits, as shaped by past ecological and evolutionary processes, may constrain future adaptive evolution. A number of studies have now considered the heritability of and covariation among traits and how these may affect their joint evolution (Lynch & Walsh, 1998; Conner & Hartl, 2004). However, typically traits related to only one particular function are examined, such as covariation among physiological (Caruso et al., 2005) or floral traits (Conner et al., 2003). A recent review convincingly argued that more studies are needed that measure traits with disparate function to understand how traits genetically covary, influence important ecological interactions (e.g. herbivory) and potentially constrain future adaptive evolution (Geber & Griffen, 2003).

Two related approaches have been used to understand the evolutionary ecology of functional traits. One recent comparative approach involves studying how functionally related traits may covary to form suites of traits or “syndromes”. This approach has been applied to such disparate topics as the coexistence of species, community assembly, pollination ecology (Grime, 1977; Chapin et al., 1993; Westoby et al., 2002; Fenster et al., 2004), and more recently, resistance against herbivores (Kursar & Coley, 2003; Agrawal & Fishbein, 2006). Another approach, typically employed at the intraspecific level, is quantitative genetics. Here, measures of variation and covariation among multiple traits are used to estimate a phenotypic (P-matrix) or genetic (G-matrix) variance-covariance matrix (Lande, 1979; Falconer & Mackay, 1996), which provides a statistical framework to predict multivariate evolution of traits in response to selection (Lande & Arnold, 1983; Rausher, 1992). Because syndromes must originate via past selection on populations, it is necessary to examine selection and associations among traits to understand the evolutionary forces that give rise to such syndromes.

Here we used a field experiment to examine 24 traits from the native plant, Common Evening Primrose (Oenothera biennis).. We measured traits that influence ecophysiology, life-history, resistance to herbivores, and morphology. Specifically, we asked the following questions: 1) What is the heritability, and 2) multivariate genetic covariation of plant traits associated with diverse functions? 3) Do single traits or multivariate suites of traits predict resistance to herbivory? 4) Is there evidence for natural selection on individual and/or multivariate suites of traits?

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