Jon Ågren

Population Size, Pollinator Limitation, and Seed Set in the Self‐ Incompatible Herb Lythrum Salicaria

In reward-producing animal-pollinated plants, small populations are likely to be less attractive to pollinators than large populations. The likelihood of pollinator limitation of seed production should therefore increase with decreasing population size. I documented the number of flowering plants and plant fecundity in 18 populations of the self-incompatible, tristylous herb Lythrum salicaria within an archipelago in northern Swe- den in two consecutive years. To test the hypothesis that a positive correlation between population size and seed set is due to a higher degree of pollinator limitation in small than in large populations, I performed supplemental hand-pollinations in eight (1993) and 13 (1994) of the study populations. To test the hypothesis that common mating types are more likely than rare types to experience inadequate pollination, I compared the natural level of seed production and the effect of supplemental pollination in different style morphs in the five populations in which -10 plants per morph were included in the experiment. There was no significant correlation between population size and plant size in terms of number of floral shoots or number of flower-producing leaf nodes per shoot. However, there was a positive relationship between population size and seed production per flower and between population size and total seed number per plant. In contrast, there was no significant correlation between population size and seed production of flowers that had received sup- plemental pollination. In both years, the difference in mean seed production per flower between hand-pollinated flowers and controls decreased with increasing population size. In two of five populations, the effect of supplemental pollination differed significantly among morphs. Seed production was more likely to be pollinator limited in long-styled than in short-styled plants, but this difference could not be attributed to a preponderance of the long-styled morph in the studied populations. Results of the supplemental hand- pollinations indicate that the positive correlation between population size and seed pro- duction is a function of insufficient pollen transfer in small populations. Additional de- mographic studies are needed to determine to what extent the reduced level of seed pro- duction in small populations limits the growth of young populations, and to what extent it may threaten the local persistence of L. salicaria.

POLLINATION SUCCESS IN A DECEPTIVE ORCHID IS ENHANCED BY CO-OCCURRING REWARDING MAGNET PLANTS

It has been debated whether pollination success in nonrewarding plants that flower in association with nectar-producing plants will be diminished by competition for pollinator visits or, alternatively, enhanced through increased local abundance of pollinators (the magnet species effect). We experimentally evaluated these effects using the nonrewarding bumblebee-pollinated orchid Anacamptis morio and associated nectar-producing plants at a site in Sweden. Pollination success (estimated as pollen receipt and pollen removal) in A. morio was significantly greater for individuals translocated to patches of nectar-producing plants (Geum rivale and Allium schoenoprasum) than for individuals placed outside (∼20 m away) such patches. These results provide support for the existence of a facilitative magnet species effect in the interaction between certain nectar plants and A. morio. To determine the spatial scale of these interactions, we correlated the visitation rate to flowers of A. morio with the density of sym...

The Scale of Population Structure in Arabidopsis thaliana

The population structure of an organism reflects its evolutionary history and influences its evolutionary trajectory. It constrains the combination of genetic diversity and reveals patterns of past gene flow. Understanding it is a prerequisite for detecting genomic regions under selection, predicting the effect of population disturbances, or modeling gene flow. This paper examines the detailed global population structure of Arabidopsis thaliana. Using a set of 5,707 plants collected from around the globe and genotyped at 149 SNPs, we show that while A. thaliana as a species self-fertilizes 97% of the time, there is considerable variation among local groups. This level of outcrossing greatly limits observed heterozygosity but is sufficient to generate considerable local haplotypic diversity. We also find that in its native Eurasian range A. thaliana exhibits continuous isolation by distance at every geographic scale without natural breaks corresponding to classical notions of populations. By contrast, in North America, where it exists as an exotic species, A. thaliana exhibits little or no population structure at a continental scale but local isolation by distance that extends hundreds of km. This suggests a pattern for the development of isolation by distance that can establish itself shortly after an organism fills a new habitat range. It also raises questions about the general applicability of many standard population genetics models. Any model based on discrete clusters of interchangeable individuals will be an uneasy fit to organisms like A. thaliana which exhibit continuous isolation by distance on many scales.

OUTCROSSING RATE AND INBREEDING DEPRESSION IN TWO ANNUAL MONOECIOUS HERBS, BEGONIA HIRSUTA AND B. SEMIOVATA

Most models of mating‐system evolution predict inbreeding depression to be low in inbred populations due to the purging of deleterious recessive alleles. This paper presents estimates of outcrossing rates and inbreeding depression for two highly selfing, monoecious annuals Begonia hirsuta and B. semiovata. Outcrossing rates were estimated using isozyme polymorphisms, and the magnitude of inbreeding depression was quantified by growing progeny in the greenhouse produced through controlled selfing and outcrossing. The estimated single‐locus outcrossing rate was 0.03 ± 0.01 (SE) for B. hirsuta and 0.05 ± 0.02 for B. semiovata. In both species, the seed production of selfed flowers was on average 12% lower than that of outcrossed flowers (B. hirsuta P = 0.07, B. semiovata P < 0.05, mixed model ANOVAs). There was no significant effect of crosstype on germination rate or survival, but selfed offspring had a lower dry mass than outcrossed offspring 18 weeks after planting in both species (on average 18% lower in B. hirsuta and 31% lower in B. semiovata). Plants that were the products of selfing began flowering later than plants produced through outcrossing in B. semiovata, but not in B. hirsuta. The effects of crosstype on seed production (B. semiovata), days to first flower and offspring dry mass (both species) varied among maternal parents, as indicated by significant crosstype x maternal parent interactions for these characters. Both species showed significant inbreeding depression for total fitness (estimated as the product of seed production, germination rate, survival and dry mass at 18 weeks). In B. hirsuta, the average total inbreeding depression was 22% (range ‐57%‐98%; N = 23 maternal parents), and in B. semiovata, it was 42% (‐11%‐84%; N = 21). This study demonstrates that highly selfing populations can harbor substantial inbreeding depression. Our findings are consistent with the hypothesis that a high mutation rate to mildly deleterious alleles contributes to the maintenance of inbreeding depression in selfing populations.

ASSOCIATIONAL RESISTANCE: INSECT DAMAGE TO PURPLE LOOSESTRIFE REDUCED IN THICKETS OF SWEET GALE

Associational resistance occurs when herbivore damage to a focal plant is reduced by the presence of other plant species. Neighboring plants can reduce herbivore damage (1) by their effects on the predator community, (2) by reducing the ability of herbivores to find their host plants, and (3) by reducing the time herbivores remain on their host plants. We examined how the presence of the aromatic low shrub Myrica gale and of predatory lady beetles affected herbivore damage and reproductive output in a population of the perennial herb Lythrum salicaria in northern Sweden. An observational study showed that L. salicaria growing in Myrica thickets were less damaged by herbivores, had a lower abundance of the monophagous, leaf-feeding, chrysomelid beetle Galerucella calmariensis, and had higher flower and seed production than L. salicaria outside Myrica thickets. To test whether these differences could be explained by (a) differences in some aspect of plant quality, or (b) differences in predator abundance, we placed potted L. salicaria within and outside Myrica thickets. To determine whether differences in the abundance of G. calmariensis were primarily the result of different rates of colonization or emigration, we marked adult beetles and placed them on a second set of potted plants in the two microhabitats. The results show that differences in herbivore abundance, plant damage, and reproductive output between potted L. salicaria placed within and outside Myrica thickets were in the same direction and of the same magnitude as those observed for naturally occurring plants, indicating that the observed patterns were not an effect of differences in the chemical composition of the host plant. Moreover, we found no support for the hypothesis that a higher abundance of insect predators could explain the lower abundance of G. calmariensis on L. salicaria in Myrica thickets. On the contrary, lady beetles (Coccinella quinqempunctata and Coccinella septempunctata) were observed on a greater proportion of the plants placed outside the Myrica thickets. The monitoring of marked beetles indicated that differences in the abundance of G. calmariensis were the result of a markedly higher colonization rate and a somewhat lower emigration rate from L. salicaria outside Myrica thickets. Outside the Myrica thickets, the survival of G. calmariensis and the magnitude of herbivore damage were lower, and fruit and seed output were higher on plants with observations of lady beetles than on plants without lady beetles. The results indicate that the abundance of the specialist herbivore G. calmariensis, and the herbivore damage and reproductive output of its host plant, L. salicaria, are affected both by the presence of the nonhost Myrica and by predation from lady beetles. We suggest that the most likely mechanism causing decreased feeding on L. salicaria growing in Myrica thickets is that Myrica affects the ability of G. calmariensis to find its host, either through visual or olfactory interference.

Latitudinal population differentiation in phenology, life history and flower morphology in the perennial herb Lythrum salicaria

Abstract In plants with a wide distribution, phenological characters can be expected to vary clinally along climatic gradients, whereas other characters important for adaptation to local biotic and abiotic factors may vary in a more mosaic fashion. We used common‐garden experiments and controlled crosses to examine population differentiation in phenology, life history and morphology in the perennial herb Lythrum salicaria along a latitudinal transect through Sweden (57°N to 66°N). Northern populations initiated growth and flowering earlier, flowered for a shorter period, were shorter, produced more and larger winter buds, and were older at first reproduction than southern populations. Flower morphology varied significantly among populations, but was, with the exception of calyx length, not significantly related to latitude of origin. Survival in the common garden (at 63°49′N) was positively correlated with latitude of origin and the size and number of winter buds produced in the preceding year. The results suggest that the among‐population differences in phenology and life history have evolved in response to latitudinal variation in length of the growing season. Further studies are required to determine whether population differentiation in flower morphology is maintained by selection.

SEXUAL DIFFERENCES IN BIOMASS AND NUTRIENT ALLOCATION IN THE DIOECIOUS RUBUS CHAMAEMORUS

I compared the seasonal pattern of biomass distribution and amounts of N and P in male and female ramets of the dioecious perennial herb Rubus chamaemorus L. Two populations, one in an open and one in a shaded habitat, were studied for 2 yr. The cost of fruit production in terms of reduction in vegetative growth was estimated in a field experiment. Ramets were larger, but the proportions of aboveground biomass, N, and P that were allocated to reproduction were lower at the shaded site than at the open site. The annual aboveground shoot ofR. chamaemorus is either single-flowered or nonfloral. Female flowers had a lower dry mass and nutrient content than had male flowers. However, the ripe fruit had a dry mass, and a content of N and P, several times as great as those of male flowers. Fruit production interfered with vegetative growth; fruit-producing female ramets produced smaller leaves, and began producing rhizome branchlets later, than male ramets and than female ramets whose flowers had been excised to prevent fruit development. Fruit-pro- ducing female ramets had a higher mortality, and a lower probability of flowering in the subsequent year, than had male ramets. The sexual differences in vegetative growth and ramet mortality were smaller in the shaded than in the open habitat. In the shaded habitat, - 50% of the ramets on male clones, and - 30% of the ramets on female clones, were floral. The results suggest that male reproductive effort is greater than female up to the time of flowering, but that the total female allocation to reproduction is greater than the total male even at relatively low levels of fruit set. The predominance of R. chamaemorus populations with male-biased floral sex ratios is proposed to be the result of males having both a greater competitive vigor and a higher flowering propensity than females.

Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range

To quantify adaptive differentiation in the model plant Arabidopsis thaliana, we conducted reciprocal transplant experiments for five years between two European populations, one near the northern edge of the native range (Sweden) and one near the southern edge (Italy). We planted seeds (years 1-3) and seedlings (years 4-5), and estimated fitness as the number of fruits produced per seed or seedling planted. In eight of the 10 possible site × year comparisons, the fitness of the local population was significantly higher than that of the nonlocal population (3.1-22.2 times higher at the southern site, and 1.7-3.6 times higher at the northern site); in the remaining two comparisons no significant difference was recorded. At both sites, the local genotype had higher survival than the nonlocal genotype, and at the Italian site, the local genotype also had higher fecundity. Across years, the relative survival of the Italian genotype at the northern site decreased with decreasing winter soil temperature. The results provide evidence of strong adaptive differentiation between natural populations of A. thaliana and indicate that differences in tolerance to freezing contributed to fitness variation at the northern site. In ongoing work, we explore the functional and genetic basis of this adaptive differentiation.

The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio.

It has been suggested that the absence of floral rewards in many orchid species causes pollinators to probe fewer flowers on a plant, and thus reduces geitonogamy, i.e. self–pollination between flowers, which may result in inbreeding depression and reduced pollen export. We examined the effects of nectar addition on pollinator visitation and pollen transfer by tracking the fate of colour–labelled pollen in Anacamptis morio, a non–rewarding orchid species pollinated primarily by queen bumble–bees. Addition of nectar to spurs of A. morio significantly increased the number of flowers probed by bumble–bees, the time spent on an inflorescence, pollinarium removal and the proportion of removed pollen involved in self–pollination through geitonogamy, but did not affect pollen carryover (the fraction of a pollinarium carried over from one flower to the next). Only visits that exceeded 18 s resulted in geitonogamy, as this is the time taken for removed pollinaria to bend into a position to strike the stigma. A mutation for nectar production in A. morio would result in an initial 3.8–fold increase in pollinarium removal per visit, but also increase geitonogamous self–pollination from less than 10% of pollen depositions to ca. 40%. Greater efficiency of pollen export will favour deceptive plants when pollinators are relatively common and most pollinaria are removed from flowers or when inbreeding depression is severe. These findings provide empirical support both for Darwins contention that pollinarium bending is an anti–selfing mechanism in orchids and for the idea that floral deception serves to maximize the efficiency of pollen export.

Variation in trichome density and resistance against a specialist insect herbivore in natural populations of Arabidopsis thaliana

Abstract.  1. The annual herb Arabidopsis thaliana is a prime model organism of plant molecular genetics, and is currently used to explore the molecular basis of resistance to herbivores. However, both the magnitude and the causes of variation in resistance among natural populations of A. thaliana are poorly known. The hypotheses (a) that resistance to a specialist herbivore, the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is positively related to the density of leaf trichomes, and (b) that oviposition preference by female moths is positively correlated to larval performance on different populations and maternal lines of the host plant were examined.