Selection on quantitative trait loci (QTL) may vary among natural environments due to differences in the genetic architecture of traits, environment-specific allelic effects or changes in the direction and magnitude of selection on specific traits. To dissect the environmental differences in selection on life history QTL across climatic regions, we grew a panel of interconnected recombinant inbred lines (RILs) of Arabidopsis thaliana in four field sites across its native European range. For each environment, we mapped QTL for growth, reproductive timing and development. Several QTL were pleiotropic across environments, three colocalizing with known functional polymorphisms in flowering time genes (CRY2, FRI and MAF2-5), but major QTL differed across field sites, showing conditional neutrality. We used structural equation models to trace selection paths from QTL to lifetime fitness in each environment. Only three QTL directly affected fruit number, measuring fitness. Most QTL had an indirect effect on fitness through their effect on bolting time or leaf length. Influence of life history traits on fitness differed dramatically across sites, resulting in different patterns of selection on reproductive timing and underlying QTL. In two oceanic field sites with high prereproductive mortality, QTL alleles contributing to early reproduction resulted in greater fruit production, conferring selective advantage, whereas alleles contributing to later reproduction resulted in larger size and higher fitness in a continental site. This demonstrates how environmental variation leads to change in both QTL effect sizes and direction of selection on traits, justifying the persistence of allelic polymorphism at life history QTL across the species range.
Floral nectar of many plant species is prone to colonization by microbial organisms such as yeasts. Their presence and metabolism of nectar chemical components have the potential to modify a suite of floral traits important for pollinator attraction, including nectar quality and scent. However, studies on the direct and indirect effects of nectar-inhabiting microorganisms on pollinator behavior and plant reproductive success remain rare. To determine their potential to affect pollinator behavior and plant fitness, we experimentally manipulated the common nectar-inhabiting yeast Metschnikowia reukaufii in the nectar of Delphinium nuttallianum, a short-lived montane perennial herb. We detected positive, indirect, pollinator-mediated effects of yeasts on male plant fitness measured as pollen donation using powdered fluorescent dyes. However, we detected no direct or indirect effects on components of female fitness. Matching effects on male plant fitness, pollinators responded positively to the presence of yeasts, removing more nectar from flowers treated with M. reukaufii. Our results provide evidence of effects of nectar-inhabiting yeasts on male plant fitness and highlight the importance of microorganisms in mediating plant-pollinator interactions and subsequent plant fitness.
Summary Pollinators utilize floral resources that vary in colour, scent and reward quality. Variation in such traits, including nectar rewards, in addition to cues associated with their quality, can influence pollinator foraging decisions with consequences for pollinator reproductive success. Nectar is commonly subject to colonization by micro‐organisms capable of affecting a suite of traits important for pollinator attraction and fitness; yet, links between microbial presence and changes in pollinator preference and performance remain few. Here, we evaluated the effects of a nectar‐inhabiting micro‐organism on pollinator foraging behaviour and reproduction using the common eastern bumblebee Bombus impatiens and the cosmopolitan nectar yeast Metschnikowia reukaufii. Using a combination of choice and no‐choice behavioural and feeding assays, we manipulated the presence and viability of M. reukaufii in nectar and assessed bumblebee foraging and reproductive responses. Bombus impatiens workers responded positively to the presence of yeasts. Foragers trained to associate yeast presence with flower colour visited a significantly greater proportion of flowers inoculated with yeast when subject to a colour discrimination test. Moreover, foragers naïve to nectar yeasts incorporated more yeast‐inoculated flowers into initial foraging bouts when presented with a novel floral array. In addition, bees spent significantly longer foraging on yeast‐inoculated flowers compared to yeast‐free flowers. However, when we manipulated yeast presence and viability in microcolonies of queenless workers, we found no effect of yeast on components of bumblebee reproduction, such as initiation of egg laying and number of eggs laid. This lack of an effect of yeast persisted even under conditions of pollen limitation. Taken together, these results suggest that nectar yeasts can enhance floral signalling and alter pollinator foraging behaviour at individual flowers, though they may not directly affect pollinator performance. Thus, nectar yeasts may play a significant role in mediating pollinator foraging behaviour, with consequences for plant fitness and evolution of floral traits.
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