Aboveground plant performance is strongly influenced by belowground microorganisms, some of which are pathogenic and have negative effects, while others, such as nitrogen-fixing bacteria and arbuscular mycorrhizal fungi, usually have positive effects. Recent research revealed that belowground interactions between plants and functionally distinct groups of microorganisms cascade up to aboveground plant associates such as herbivores and their natural enemies. However, while functionally distinct belowground microorganisms commonly co-occur in the rhizosphere, their combined effects, and relative contributions, respectively, on performance of aboveground plant-associated organisms are virtually unexplored. Here, we scrutinized and disentangled the effects of free-living nitrogen-fixing (diazotrophic) bacteria Azotobacter chroococcum (DB) and arbuscular mycorrhizal fungi Glomus mosseae (AMF) on host plant choice and reproduction of the herbivorous two-spotted spider mite Tetranychus urticae on common bean plants Phaseolus vulgaris. Additionally, we assessed plant growth, and AMF and DB occurrence and density as affected by each other. Both AMF alone and DB alone increased spider mite reproduction to similar levels, as compared to the control, and exerted additive effects under co-occurrence. These effects were similarly apparent in host plant choice, that is, the mites preferred leaves from plants with both AMF and DB to plants with AMF or DB to plants grown without AMF and DB. DB, which also act as AMF helper bacteria, enhanced root colonization by AMF, whereas AMF did not affect DB abundance. AMF but not DB increased growth of reproductive plant tissue and seed production, respectively. Both AMF and DB increased the biomass of vegetative aboveground plant tissue. Our study breaks new ground in multitrophic belowground–aboveground research by providing first insights into the fitness implications of plant-mediated interactions between interrelated belowground fungi–bacteria and aboveground herbivores.

Polyandry is more widespread than anticipated from Bateman’s principle but its ultimate (evolutionary) causes and proximate (mechanistic) correlates are more difficult to pinpoint than those of polygyny. Here, we combined mating experiments, quantification of reproductive traits and microsatellite genotyping to determine the fitness implications of polyandry in two predatory mite species, where males are highly polygynous (up to 45 fertilized females during life), whereas females range from monandry to various polyandry levels. The medium-level polyandrous (up to eight male mates possible) Neoseiulus californicus received clear direct and indirect benefits: multiply mated females produced more offspring with higher survival chances over longer times than singly mated females. In contrast, singly and multiply mated females of the low-level polyandrous (commonly two male mates at maximum) Phytoseiulus persimilis produced similar numbers of offspring having similar survival chances. In both species, multiple mating resulted in mixed offspring paternities, opening the chance for indirect fitness benefits such as enhanced genetic compatibility, complementarity and/or variability. However, the female re-mating likelihood and the paternity chance of non-first male mates were lower in P. persimilis than in N. californicus. Regarding proximate factors, in both species first mating duration and female re-mating likelihood were negatively correlated. Based on occasional fertilization failure of first male mates in P. persimilis, and mixed offspring paternities in both species, we argue that fertilization assurance and the chance to gain indirect fitness benefits are the ultimate drivers of polyandry in P. persimilis, whereas those of N. californicus are higher offspring numbers coupled with enhanced offspring viability and possibly other indirect fitness benefits. Overall, the adaptive significance and proximate events well reflected the polyandry levels. Our study provides a key example for linking behavioral experiments, quantification of reproductive traits and paternity analysis via offspring genotyping to explain the evolution of differing levels of polyandry.

Symbiotic root micro-organisms such as arbuscular mycorrhizal fungi commonly change morphological, physiological and biochemical traits of their host plants and may thus influence the interaction of aboveground plant parts with herbivores and their natural enemies. While quite a few studies tested the effects of mycorrhiza on life history traits, such as growth, development and reproduction, of aboveground herbivores, information on possible effects of mycorrhiza on host plant choice of herbivores via constitutive and/or induced plant volatiles is lacking. Here we assessed whether symbiosis of the mycorrhizal fungus Glomus mosseae with common bean plants Phaseolus vulgaris influences the response of the two-spotted spider mite Tetranychus urticae to volatiles of plants that were clean or infested with spider mites. Mycorrhiza-naïve and -experienced spider mites, reared on mycorrhizal or non-mycorrhizal bean plants for several days before the experiments, were subjected to Y-tube olfactometer choice tests. Experienced but not naïve spider mites distinguished between constitutive volatiles of clean non-mycorrhizal and mycorrhizal plants, preferring the latter. Neither naïve nor experienced spider mites distinguished between spider mite-induced volatiles of mycorrhizal and non-mycorrhizal plants. Learning the odor of clean mycorrhizal plants, resulting in a subsequent preference for these odors, is adaptive because mycorrhizal plants are more favorable host plants for fitness of the spider mites than are non-mycorrhizal plants.