Philaenus Spumarius) Herbivory in Mimulus Guttatus
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Heredity (2009) 102, 303–311 & 2009 Macmillan Publishers Limited All rights reserved 0018-067X/09 $32.00 www.nature.com/hdy ORIGINAL ARTICLE Genetic variation and constraints on the evolution of defense against spittlebug (Philaenus spumarius) herbivory in Mimulus guttatus CT Ivey1, DE Carr2 and MD Eubanks3 1Department of Biological Sciences, California State University, Chico, CA, USA; 2Blandy Experimental Farm, University of Virginia, Boyce, VA, USA and 3Department of Entomology, Texas A and M University, College Station, TX, USA Plants mediate carbon into most ecosystems and are thus variation for tolerance to herbivory except for a small non- under persistent attack by diverse enemies. The evolution of nuclear paternal contribution to tolerance for flower number. defense against such assaults will depend on the availability Additive genetic correlations indicated that more resistant of genetic variation, as well as the costs and constraints on plant genotypes (in terms of adult spittlebug biomass) were defense. We estimated the magnitude of genetic variation for also smaller in the absence of spittlebugs, suggesting a defense against spittlebug (Philaenus spumarius) herbivory potential cost of resistance to herbivory. We found no other in Mimulus guttatus using a diallel cross-grown in a green- significant genetic correlations indicating a cost of defense, house. Except for flowering time, additive genetic variation nor did we find evidence for a tradeoff between resistance for the plant traits we measured was negligible, regardless of and tolerance to herbivory. Overall, these results suggest herbivory environment. In contrast, nonadditive genetic the future adaptive evolution of tolerance to spittlebugs in variation contributed significantly to all plant traits measured. this population will be limited primarily by available We found significant additive genetic variation among plants genetic variation, whereas the future evolution of antibiosis for biomass of adult spittlebugs, suggesting heritability for resistance may be constrained by allocation costs of resistance to herbivory. The other putative resistance trait resistance. measured, spittlebug maturation time, was not significantly Heredity (2009) 102, 303–311; doi:10.1038/hdy.2008.122; heritable. We found no evidence for significant genetic published online 17 December 2008 Keywords: diallel; genetic correlation; herbivory; Mimulus guttatus; resistance; tolerance Introduction strategy is expected (van der Meijden et al., 1988). Selection for tolerance, for example, is expected to be Plants are the primary source of carbon and energy for weak on a highly resistant genotype, because the two most other organisms, and as a consequence, they are forms of defense are considered to be redundant under persistent attack by natural enemies. A wide (Fineblum and Rausher, 1995). The evolution of defense, variety of strategies for limiting the impact of consumers therefore, can be constrained by low genetic variation or can be found among plants. These defense phenotypes by genetic correlations with other traits on which have been broadly categorized into two forms. ‘Resis- selection acts in opposition. tance’ includes traits that limit enemy attack (antixeno- A number of earlier studies have contributed toward sis) or performance (antibiosis), whereas ‘tolerance’ our understanding of genetic variation and constraints in describes traits that affect the performance of plants herbivore defense by using clonal (Marquis, 1990; Wise, under attack (Strauss and Agrawal, 1999). 2007) or half-sib (Maddox and Root, 1987; Fornoni et al., In general, some form of defense is expected to evolve 2003) experimental designs (reviewed in Berenbaum and in response to attack by an enemy if there is a fitness cost Zangerl, 1992; Kennedy and Barbour, 1992). These exacted by the attack. In the absence of genetic variation approaches, however, cannot partition genetic variation for traits conferring resistance or tolerance, however, from most nonadditive sources, such as epistatic or defense will not evolve. In addition, the evolution of dominance variation, or non-nuclear parental effects defensive traits may be constrained if their development (Lynch and Walsh, 1998). Any substantial contribution requires resources that would otherwise contribute by these other sources of genetic variation could inflate toward growth or reproduction (Strauss et al., 2002). the estimate of heritability in such studies and lead to Under such circumstances some specialization in defense misinterpretation of the potential response of traits to natural selection. Nonadditive genetic variation for defense is routinely reported for crop species (Soper Correspondence: Dr CT Ivey, Department of Biological Sciences, et al., 1984; Wilson, 1990; Dhliwayo et al., 2005), but very California State University, Chico, 205 Holt Hall, Chico, CA, few studies of defense in natural systems have used 95929-0515, USA. E-mail: [email protected] experimental designs that can reveal nonadditive genetic Received 19 June 2008; revised 22 October 2008; accepted variation (but see Simms and Rausher, 1987; Juenger and 11 November 2008; published online 17 December 2008 Bergelson, 2000). Genetic variation for herbivory defense in Mimulus CT Ivey et al 304 We used a diallel breeding design to estimate genetic recipient to perform hand-pollinations. Each fruit ma- variation and constraints on the evolution of resistance tured resulted in several hundred full-sibling seeds. (antibiosis) and tolerance to herbivory by spittlebugs Approximately 50 seeds from each cross were sown into (Philaenus spumarius L., Cercopidae:Homoptera) in a separate 71-mm pots, from which 12 emerging seedlings population of yellow monkey flower (Mimulus guttatus were randomly chosen to include in the diallel experi- DC, Phrymaceae, formerly Scrophulariaceae). The pri- ment, resulting in a total of 2700 plants. Seedlings were mary aims of our study were (1) to estimate the transplanted at the cotyledon stage into individual magnitude of additive and nonadditive genetic compo- 71-mm pots. Two plants from each cross were randomly nents of resistance and tolerance to spittlebug herbivory, assigned to positions within each of six greenhouse (2) to test for constraints on the evolution of defense by benches (blocks), and one plant from each pair was estimating genetic correlations between defense and randomly assigned to receive a second instar spittlebug plant fitness components and (3) to test for constraints nymph. Spittlebugs were applied to plants during the on defense strategies by estimating the genetic correla- rosette stage, which is the developmental stage of tion between resistance and tolerance. M. guttatus during early spring when spittlebug colonization typically occurs. Spittlebugs generally began to feed on plants within minutes of application, and they were Materials and methods allowed to feed until they emerged as adults. Adult spittlebugs were collected at emergence, dried at 50 1C Study system for 2 days, and weighed on a Cahn C-31 microbalance to M. guttatus is an herb native to open, wet habitats the nearest 0.001 mg. We recorded the number of days throughout much of western North America. It produces after transplanting when each plant opened its first many perfect yellow flowers that are typically paired at flower (days to first flower, DFF). After all spittlebugs nodes along erect racemes. Each flower can produce had been collected, we counted the number of flowers several hundred seeds. M. guttatus is an annual, except in produced by each plant. In addition, all above-ground some sites that remain wet year-round, where it can plant biomass was dried to constant weight at 50 1C and persist throughout the year and spread rhizomatously weighed to the nearest 0.01 g. (Dole, 1992). The mating system of M. guttatus varies from approximately 75% selfing (t ¼ 0.25) to complete Analyses E outcrossing (t ¼ 1.0), with a species mean t 0.6 (Ritland To correct for heteroskedasticity, plant and insect and Ritland, 1989; Dudash and Ritland, 1991; Willis, biomass data were natural log-transformed and count 1993). Inbreeding depression is commonly observed in data (DFF, number of flowers and number of days to M. guttatus (Carr and Dudash, 1996; Carr and Eubanks, spittlebug maturation) were squareroot transformed 2002; Ivey et al. 2004). Voucher specimens of native plants before the analyses. The effect of spittlebugs on plant from the population studied herein (M13: Napa County, biomass and flower number was evaluated using mixed- 1 0 1 0 California, USA, 38 33 N, 122 22 W) are housed in the model analysis of variance in which dam and block were Illinois Natural History Survey herbarium. random effects and herbivory treatment was the fixed The meadow spittlebug, P. spumarius, is a widespread effect. generalist herbivore that feeds on xylem (Weaver and Plant performance (number of flowers and plant King, 1954). Spittlebugs were the most abundant biomass) was used to estimate plant tolerance (T)to herbivore species in our coastal California study sites. herbivory as T ¼ D–U, where D ¼ fitness of the damaged Infested plants typically hosted 1–2 spittlebug nymphs, plant and U ¼ fitness of the undamaged plant (Strauss and fewer than half of plants hosted spittlebugs (CT Ivey and Agrawal, 1999). Negative values thus suggest a and DE Carr, personal observation). A single spittlebug fitness cost to herbivory, whereas positive values indicate nymph can exact significant costs to the survival and