American Journal of Botany 87(12): 1769±1777. 2000. GENETIC VARIATION AND EVOLUTIONARY TRADE-OFFS FOR SEXUAL AND ASEXUAL REPRODUCTIVE MODES IN ALLIUM VINEALE (LILIACEAE)1 MARGARET L. RONSHEIM2,3 AND JAMES D. BEVER4,5 2Department of Biology, Box 513, Vassar College, 124 Raymond Avenue, Poughkeepsie, New York 12604-0513 USA; and 4Department of Biology, Indiana University, Bloomington, Indiana 47405 USA Populations of Allium vineale commonly include individuals with very different allocation patterns to three modes of reproduction: sexual ¯owers, aerially produced asexual bulbils, and belowground asexual offsets. If selection is currently acting to maintain these different allocation patterns there must be a genetic basis for variation in allocation to these three reproductive modes. In addition, negative genetic correlations between reproductive traits would imply evolutionary trade-offs among reproductive strategies. We eval- uated the heritability of these allocation patterns by growing 16 clones from a single population in the greenhouse at two levels of fertilization. Bulb mass and the mass and number of bulbils, offsets, and ¯owers were used as response variables, in addition to the proportion allocated to each reproductive mode. We found evidence of substantial heritable variation in allocation to sexual reproduction and in allocation within the two modes of asexual reproduction, indicating high sensitivity of these allocation patterns to natural selection. We also found evidence of strong negative genetic correlations between bulbil and ¯ower traits, as well as between bulbil and offset traits, with one group of genotypes allocating greater resources to aerial asexual bulbils and the second group allocating more resources to belowground asexual offsets and aerial ¯owers. Phenotypic plasticity in allocation to above- vs. belowground asexual reproduction and sexual vs. asexual aerial reproduction was limited, indicating that plants are unlikely to change reproductive mode in response to nutrient availability. Together, then, we have demonstrated strong heritability for, and trade-offs in, the reproductive allocation patterns within this plant population. Key words: Allium vineale; genetic correlations; heritability; life history traits; Liliaceae; multiple reproductive modes; trade- offs. Diverse modes of reproduction are often maintained within tion of beaked to unbeaked achenes at lower plant density species and within single plant populations. For example, plant (Baker and O'Dowd, 1982). In general, higher light and nu- species can produce combinations of chasmogamous and cleis- trient levels increase the proportion of chasmogamous to cleis- togamous ¯owers (e.g., Impatiens, Schemske, 1978; Danthon- togamous ¯owers (e.g., Schemske, 1978; Trapp and Hendrix, ia spicata, Clay, 1982; Viola mirabilis, Mattila and Salonen, 1988; Le Corff, 1993; but see Mattila and Salonen, 1995). In 1995), aerial and subterranean seeds (e.g., Amphicarpum pur- Amphicarpum purshii, aerial reproduction occurs under higher shii, Cheplick and Quinn, 1988; Amphicarpaea bracteata, resource availability, while subterranean seeds are produced at Trapp and Hendrix, 1988; see Cheplick, 1987, for a review), all resource levels (Cheplick and Quinn, 1982). Selection seeds and ramets (e.g., Tussilago farfara, Ogden, 1974; Fra- would favor such phenotypic plasticity if different propagule garia virginiana, Holler and Abrahamson, 1977), as well as types are favored when environmental conditions change heteromorphic aerial achenes (e.g., Hypochoeris glabra, Baker (Schoen and Lloyd, 1984; Loehle, 1987). and O'Dowd, 1982; Heterosperma pinnatum, Venable and In order for natural selection to currently operate to maintain Burquez, 1989). Adaptive explanations for the maintenance of these diverse reproductive strategies and phenotypic plasticity this diversity posit trade-offs among alternate components of in allocation patterns, the variation in reproductive mode must ®tness. For example, some propagule types may be favored in have a genetic basis. In fact, the response of a population competitive situations near the parent, while others may serve depends not only on the availability of genetic variation, but a role in dispersal (Schoen and Lloyd, 1984; Venable, 1985). also on the existence of genetic correlations between traits Different advantages may also exist for producing sexual vs. (Reznick, 1985). In particular, negative genetic correlations be- asexual progeny, as sexual progeny may be favored in the tween life history traits suggest trade-offs in reproductive strat- presence of pathogens or changing environments, and asexual egies (Falconer, 1981; Stearns, 1992), as selection for in- progeny may be favored in static environments. creased allocation to one trait will cause a decrease in allo- In addition, genotypes are known to vary their allocation to cation to the other. different modes of reproduction with environmental change. In general, reproductive traits have lower heritabilities than Allocation to vegetative and sexual reproduction changes with morphological traits (Mousseau and Roff, 1987), but signi®- plant density in several species (e.g., Ogden, 1974; Abraham- cant genetic variation in allocation to different reproductive son, 1975; Holler and Abrahamson, 1977; for a review see modes has been demonstrated (e.g., cleistogamy vs. chasmo- Loehle, 1987). Hypochoeris glabra produces a higher propor- gamy, Clay, 1982; proportion of achene morphs, Venable and Burquez, 1989; allocation to aerial seeds, Cheplick and Quinn, 1 Manuscript received 22 June 1999; revision accepted 29 February 2000. 1988). Negative genetic correlations, which indicate trade-offs The authors thank Kathy Mills, Sarah Cross, and Shawn White and ac- among life history traits, have also been detected. For exam- knowledge support from USDA grants 92-37101-7461 and 94-37101-0354 and NSF grant DEB 9996221. ple, Law (1979) found a negative correlation between ®rst- 2 Author for correspondence (e-mail: [email protected]). and second-year reproduction in Poa annua, and Campbell 3 e-mail: [email protected]. (1997) observed a negative correlation between corolla width, 1769 1770 AMERICAN JOURNAL OF BOTANY [Vol. 87 which affects pollen export rates and potentially male ®tness, and others that do produce ¯owers have low seed set, measurement of heri- and net female ®tness. However, not all species demonstrate tability through maternal or paternal contributions would be dif®cult and not trade-offs in life history strategies (see Stearns, 1992, for a representative of the natural population. Instead, we have measured the broad- review). For example, Cain et al. (1995) found no evidence sense or clonal heritabilities and correlations by using the aerially produced for genetic trade-offs among ®ve reproductive traits in Trifo- asexual bulbils to replicate genotypes. This approach has the obvious limi- lium repens, and Weis, Hollenbach, and Abrahamson (1987) tation that we are not able to separate the additive genetic variance compo- found only indirect evidence for a trade-off between sexual nents from the dominance, epistatic, or maternal components. Furthermore, and asexual reproduction in Solidago altissima. In addition, in sampling the population we were not able to include individuals that pro- the presence of trade-offs may be dependent on resource avail- duce in¯orescences with ¯owers and no bulbils (a small minority in this pop- ability, with stronger allocation trade-offs present when nutri- ulation), which may reduce the genetic variation that we measure. We also ents are more limiting (e.g., Reznick, 1985; Biere, 1995; purposefully collected bulbils from two groups of individuals: one that pro- duced some ¯owers and a second that produced only bulbils. This resulted in Schlichting and Pigliucci, 1998) a higher representation in our study than in the ®eld of individuals that pro- Our study organism, Allium vineale, has three modes of re- duce both ¯owers and bulbils in their in¯orescence, and may in¯ate our es- production, each with its own implications for genetic vari- timate of genetic variance. While these sampling dif®culties reduce the rele- ability, dispersal, dormancy, and probability of successful es- vance of our measured values of heritabilities and genetic correlations to the tablishment. Two of the modes are asexual in nature, one being population of their origin, these estimates are still valuable to address the aboveground (bulbils), the other belowground (offsets). Sex- issue of the evolutionary potential within Allium populations in general. ually produced aerial seeds are the third type of propagule. In this experiment we determined the reproductive allocation of replicates Within one population, it is possible to ®nd individuals that of 16 different genotypes when grown in two fertilization regimes. Infruc- are reproducing solely asexually, as well as individuals that tescences were collected in September 1993 from 16 different plants at a ®eld are reproducing both sexually and asexually, in varying pro- site in Durham, North Carolina (for details of the ®eld site, see Fowler, 1978; portions. To determine whether there is genetic variation in Fowler and Antonovics, 1981). Each of the parents was considered a separate allocation to these three reproductive modes and to test for genotype, for a total of 16 genotypes. A range of infructescence phenotypes trade-offs between sexual and asexual reproduction in Allium was included, varying from all bulbils