Nina Sletvold

Pollinator‐mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica

• Nonrewarding animal-pollinated plants commonly experience severe pollen limitation, which should result in strong selection on traits affecting the success of pollination. However, the importance of pollinators as selective agents on floral traits in deceptive species has not been quantified experimentally. • Here, we quantified pollinator-mediated selection (Δβ(poll)) on floral morphology and start of flowering in the deceptive orchid Dactylorhiza lapponica by subtracting estimates of selection gradients for plants receiving supplemental hand-pollination from estimates obtained for open-pollinated control plants. • There was directional selection for taller plants with more flowers and longer spurs, but no statistically significant selection on corolla size or flowering start. Pollinator-mediated selection accounted for all observed selection on spur length (Δβ(poll) = 0.32), 76% of the selection on plant height (Δβ(poll) = 0.19) and 42% of the selection on number of flowers (Δβ(poll = 0.30). Sixteen per cent of developing fruits were consumed by insect herbivores, but fruit herbivory had only minor effects on the strength of pollinator-mediated selection. • Our results demonstrate that pollinators mediate selection on floral traits likely to affect both pollinator attraction and pollination efficiency, and are consistent with the hypothesis that deceptive species experience strong selection for increased display and mechanical fit between flower and pollinator.

Pollinator-Mediated Selection on Floral Display and Spur Length in the Orchid Gymnadenia conopsea

Floral diversification and specialization are thought to be driven largely by interactions with pollinators, but the extent to which current selection on floral traits is mediated by pollinators has rarely been determined experimentally. We documented selection through female function on floral traits in two populations of the rewarding orchid Gymnadenia conopsea in two years and quantified pollinator-mediated selection (Δβpoll) by subtracting estimates of selection gradients for plants receiving supplemental hand pollination from estimates obtained for open-pollinated control plants. There was directional selection for taller plants, more flowers, larger corollas, and longer spurs in the study populations. Pollinator-mediated selection ranged from weak to moderately strong (Δβpoll, range −0.01–0.21, median 0.08). All observed selection on spur length could be attributed to interactions with pollinators, while the proportion of observed selection on plant height (0%–77%), number of flowers (13%–42%), and corolla size (13%–97%) caused by pollinators varied among populations and years. Our results demonstrate that pollinators can mediate selection on both traits likely to be involved in pollinator attraction and traits affecting pollination efficiency. They further show that spatiotemporal variation in the strength of pollinator-mediated selection can contribute substantially to differences in selection between years and populations.

Precipitation drives global variation in natural selection

Climate-driven selection Climate change will fundamentally alter many aspects of the natural world. To understand how species may adapt to this change, we must understand which aspects of the changing climate exert the most powerful selective forces. Siepielski et al. looked at studies of selection across species and regions and found that, across biomes, the strongest sources of selection were precipitation and transpiration changes. Importantly, local and regional climate change explained patterns of selection much more than did global change. Science, this issue p. 959 Local and regional climate changes in rainfall explain patterns of species selection across biomes more than global change. Climate change has the potential to affect the ecology and evolution of every species on Earth. Although the ecological consequences of climate change are increasingly well documented, the effects of climate on the key evolutionary process driving adaptation—natural selection—are largely unknown. We report that aspects of precipitation and potential evapotranspiration, along with the North Atlantic Oscillation, predicted variation in selection across plant and animal populations throughout many terrestrial biomes, whereas temperature explained little variation. By showing that selection was influenced by climate variation, our results indicate that climate change may cause widespread alterations in selection regimes, potentially shifting evolutionary trajectories at a global scale.

Cost of trichome production and resistance to a specialist insect herbivore in Arabidopsis lyrata.

Theory predicts that trade-offs between resistance to herbivory and other traits positively affecting fitness can maintain genetic variation in resistance within plant populations. In the perennial herb Arabidopsis lyrata, trichome production is a resistance trait that exhibits both qualitative and quantitative variation. Using a paternal half-sib design, we conducted two greenhouse experiments to ask whether trichomes confer resistance to oviposition and leaf herbivory by the specialist moth Plutella xylostella, and to examine potential genetic constraints on evolution of increased resistance and trichome density. In addition, we examined whether trichome production is induced by insect herbivory. We found strong positive genetic and phenotypic correlations between leaf trichome density and resistance to leaf herbivory, demonstrating that the production of leaf trichomes increases resistance to leaf damage by P. xylostella. Also resistance to oviposition tended to increase with increasing leaf trichome density, but genetic and phenotypic correlations were not statistically significant. Trichome density and resistance to leaf herbivory were negatively correlated genetically with plant size in the absence of herbivores, but not in the presence of herbivores. There was no evidence of increased trichome production after leaf damage by P. xylostella. The results suggest that trichome production and resistance to leaf herbivory are associated with a cost and that the direction of selection on resistance and trichome density depends on the intensity of herbivory.

Additive effects of pollinators and herbivores result in both conflicting and reinforcing selection on floral traits

Mutualists and antagonists are known to respond to similar floral cues, and may thus cause opposing selection on floral traits. However, we lack a quantitative understanding of their independent and interactive effects. In a population of the orchid Gymnadenia conopsea, we manipulated the intensity of pollination and herbivory in a factorial design to examine whether both interactions influence selection on flowering phenology, floral display, and morphology. Supplemental hand-pollination increased female fitness by 31% and one-quarter of all plants were damaged by herbivores. Both interactions contributed to selection. Pollinators mediated selection for later flowering and herbivores for earlier flowering, while both selected for longer spurs. The strength of selection was similar for both agents, and their effects were additive. As a consequence, there was no. net selection on phenology, whereas selection on spur length was strong. The experimental results demonstrate that both pollinators and herbivores can markedly influence the strength of selection on flowering phenology and floral morphology, and cause both conflicting and reinforcing selection. They also indicate that the direction of selection on phenology will vary with the relative intensity of the mutualistic and antagonistic interaction, potentially resulting in both temporal and among-population variation in optimal flowering time.

Nonadditive effects of floral display and spur length on reproductive success in a deceptive orchid

Pollinators may mediate selection on traits affecting pollinator attraction and effectiveness, and while nonadditive effects of traits influencing the two components of pollination success are expected when seed production is pollen limited, they have been little studied. In a factorial design, we manipulated one putative attraction trait (number of flowers) and one putative efficiency trait (spur length) previously shown to be subject to pollinator-mediated selection in the deceptive orchid Dactylorhiza lapponica. Removal of half of the flowers reduced pollen removal, proportion of flowers receiving pollen, fruit set, and fruit mass compared to unmanipulated plants, while spur-tip removal increased fruit set and fruit mass but did not affect pollen removal or proportion of flowers receiving pollen. The effect of spur-tip removal on fruit mass was stronger among plants with intact number of flowers compared to plants with experimentally reduced number of flowers. The results demonstrate that number of flowers and spur length are direct targets of selection and may affect female fitness nonadditively. More generally, they show that the adaptive value of a given trait can depend on floral context and illustrate how experimental approaches can advance our understanding of the evolution of trait combinations.

Separating selection by diurnal and nocturnal pollinators on floral display and spur length in Gymnadenia conopsea

Most plants attract multiple flower visitors that may vary widely in their effectiveness as pollinators. Floral evolution is expected to reflect interactions with the most important pollinators, but few studies have quantified the contribution of different pollinators to current selection on floral traits. To compare selection mediated by diurnal and nocturnal pollinators on floral display and spur length in the rewarding orchid Gymnadenia conopsea, we manipulated the environment by conducting supplemental hand-pollinations and selective pollinator exclusions in two populations in central Norway. In both populations, the exclusion of diurnal pollinators significantly reduced seed production compared to open pollination, whereas the exclusion of nocturnal pollinators did not. There was significant selection on traits expected to influence pollinator attraction and pollination efficiency in both the diurnal and nocturnal pollination treatment. The relative strength of selection among plants exposed to diurnal and nocturnal visitors varied among traits and populations, but the direction of selection was consistent. The results suggest that diurnal pollinators are more important than nocturnal pollinators for seed production in the study populations, but that both categories contribute to selection on floral morphology. The study illustrates how experimental manipulations can link specific categories of pollinators to observed selection on floral traits, and thus improve our understanding of how species interactions shape patterns of selection.

Climate warming alters effects of management on population viability of threatened species: results from a 30-year experimental study on a rare orchid

Climate change is expected to influence the viability of populations both directly and indirectly, via species interactions. The effects of large-scale climate change are also likely to interact with local habitat conditions. Management actions designed to preserve threatened species therefore need to adapt both to the prevailing climate and local conditions. Yet, few studies have separated the direct and indirect effects of climatic variables on the viability of local populations and discussed the implications for optimal management. We used 30 years of demographic data to estimate the simultaneous effects of management practice and among-year variation in four climatic variables on individual survival, growth and fecundity in one coastal and one inland population of the perennial orchid Dactylorhiza lapponica in Norway. Current management, mowing, is expected to reduce competitive interactions. Statistical models of how climate and management practice influenced vital rates were incorporated into matrix population models to quantify effects on population growth rate. Effects of climate differed between mown and control plots in both populations. In particular, population growth rate increased more strongly with summer temperature in mown plots than in control plots. Population growth rate declined with spring temperature in the inland population, and with precipitation in the coastal population, and the decline was stronger in control plots in both populations. These results illustrate that both direct and indirect effects of climate change are important for population viability and that net effects depend both on local abiotic conditions and on biotic conditions in terms of management practice and intensity of competition. The results also show that effects of management practices influencing competitive interactions can strongly depend on climatic factors. We conclude that interactions between climate and management should be considered to reliably predict future population viability and optimize conservation actions.

Vegetation context influences the strength and targets of pollinator‐mediated selection in a deceptive orchid

Clarifying the relationship between environmental context and the adaptive significance of floral traits is fundamental for an understanding of spatial and temporal variation in pollinator-mediated selection. We manipulated vegetation height and pollination regime of the orchid Dactylorhiza lapponica in a factorial design to test whether pollinator-mediated selection on floral traits is stronger in tall than in short vegetation, and whether this difference is larger for visual traits affecting pollinator attraction than for traits affecting pollination efficiency. In tall vegetation, pollinators mediated strong selection for taller plants (change in selection gradient for pollination, deltabeta(poll) = 0.33), more flowers (deltabeta(poll) = 0.34), and longer spurs (deltabeta(poll) = 0.42). In short vegetation, there was no significant selection on plant height, and pollinator-mediated selection on number of flowers and spur length was reduced by 52% and 25%, respectively. The results demonstrate experimentally that vegetation context can markedly influence the strength of pollinator-mediated selection on visual display traits, and indicate that this effect is weaker for traits affecting pollination efficiency. The study illustrates how crossed manipulations of environmental factors can reveal the causal links between ecological context and selection on floral traits.

THERE IS MORE TO POLLINATOR‐MEDIATED SELECTION THAN POLLEN LIMITATION

Spatial variation in pollinator‐mediated selection (Δβpoll) is a major driver of floral diversification, but we lack a quantitative understanding of its link to pollen limitation (PL) and net selection on floral traits. For 2–5 years, we quantified Δβpoll on floral traits in two populations each of two orchid species differing in PL. In both species, spatiotemporal variation in Δβpoll explained much of the variation in net selection. Selection was consistently stronger and the proportion that was pollinator‐mediated was higher in the severely pollen‐limited deceptive species than in the rewarding species. Within species, variation in PL could not explain variation in Δβpoll for any trait, indicating that factors influencing the functional relationship between trait variation and pollination success govern a major part of the observed variation in Δβpoll. Separating the effects of variation in mean interaction intensity and in the functional significance of traits will be necessary to understand spatiotemporal variation in selection exerted by the biotic environment.