Fitness costs of delayed pollination in a mixed-mating plant

Background and Aims To predict the evolutionary consequences of pollinator declines, we need to understand the evolution of delayed autonomous self-pollination, which is expected to evolve as a mechanism of reproductive assurance when cross-pollination becomes unreliable. This involves estimating the costs of increased levels of selfing as well as those associated with floral senescence. Methods We studied the mechanisms and costs of delayed self-pollination in the mixed-mating vine Dalechampia scandens (Euphorbiaceae) by first assessing among-population variation in herkogamy and dichogamy, which together determine the rate and timing of autonomous self-pollination. We then tested whether floral longevity responds plastically to delayed pollination. Finally, we assessed the costs of delayed self-pollination in terms of seed number and size, explicitly separating inbreeding depression from effects of floral senescence. Key Results Herkogamy varied extensively, while variation in dichogamy was more limited. Unpollinated blossoms increased their longevity, but seed quantity and quality decreased with increasing delays in pollination, independently of inbreeding depression. Conclusions In D. scandens, earlier autonomous selfing is facilitated by reduced herkogamy rather than reduced protogyny, providing reproductive assurance while maintaining the possibility for outcrossing events. Effective early autonomous self-pollination may evolve under reduced cross-pollination reliability in response to costs associated with floral senescence

Inbreeding effects in a mixed-mating vine:effects of mating history, pollen competition and stress on the cost of inbreeding

Inbreeding depression is assumed to be a central factor contributing to the stability of plant mating systems. Predicting the fitness consequence of inbreeding in natural populations is complicated, however, because it may be affected by the mating histories of populations generating variation in the amount of purging of deleterious alleles. Furthermore, the level of inbreeding depression may depend on environmental conditions and the intensity of pollen competition. In a greenhouse experiment comparing four populations of the neotropical vine Dalechampia scandens (Euphorbiaceae), we tested whether inbreeding depression for early-life fitness depended on the inferred mating history of each population, as indicated by genetically determined differences in herkogamy and autofertility rates. We also tested whether the intensity of pollen competition and the level of stress encountered by the seeds and seedlings affected the amount of inbreeding depression observed. Herkogamy was a good predictor of autofertility in each population. However, we found only limited evidence for inbreeding depression in any population, and inbreeding depression varied independently of the intensity of pollen competition and amount of stress encountered by the seeds and seedlings. Thus, the population's rate of autofertility did not predict the amount of inbreeding depression. Overall, we found no evidence supporting the expectations that more inbred populations experience less inbreeding depression, and that pollen competition reduces the cost of inbreeding. These results suggest that additional factors may be responsible for the maintenance of the mixed mating systems of D. scandens populations

Quantitative and qualitative consequences of reduced pollen loads in a mixed-mating plant

Greater pollination intensity can enhance maternal plant fitness by increasing seed set and seed quality as a result of more intense pollen competition or enhanced genetic sampling. We tested experimentally these effects by varying the pollen load from a single pollen donor on stigmas of female flowers of Dalechampia scandens (Euphorbiaceae) and measuring the effects on seed number and seed mass. Seed set increased rapidly with pollen number at low to moderate pollen loads, and a maximum set of three seeds occurred with a mean pollen load of 19 pollen grains. We did not detect a trade‐off between the number of seeds and seed mass within a fruit. Seed mass increased with increasing pollen load, supporting the hypothesis of enhanced seed quality via increased pollen‐competition intensity or genetic sampling. These results suggest that maternal fitness increases with larger pollen loads, even when the fertilization success is already high. Our results further highlight the importance of high rates of pollen arrival onto stigmas, as mediated by reliable pollinators. Comparing the pollen‐to‐seed response curve obtained in this experiment with those observed in natural populations suggests that pollen limitation may be more severe in natural populations than predicted from greenhouse studies. These results also indicate that declines in pollinator abundance may decrease plant fitness through lowered seed quality before an effect on seed set is detected.publishedVersio

No evidence that seed predators constrain pollinator-mediated trait evolution in a tropical vine

Premise of the Study: Turnover in biotic communities across heterogeneous landscapes is expected to lead to variation in interactions among plants, their mutualists, and their antagonists. Across a fragmented landscape in northern Costa Rica, populations of the euphorb vine Dalechampia scandens vary widely in mating systems and associated blossom traits. Previous work suggested that populations are well adapted to the local reliability of pollination by apid and megachilid bees. We tested whether variation in the intensity of predispersal seed predation by seed weevils in the genus Nanobaris also contributes to the observed variation in blossom traits. Methods: We studied spatiotemporal variation in the relationships between floral advertisement and the probability of seed predation within three focal populations. Then we assessed among-population covariation of predation rate, pollination reliability, mating system, and blossom traits across 20 populations. Key Results: The probability of seed predation was largely unrelated to variation in floral advertisement both within focal populations and among the larger sample of populations. The rate of seed predation was only weakly associated with the rate of cross-pollination (allogamy) in each population but tended to be proportionally greater in populations experiencing less reliable pollination. Conclusions: These results suggest that geographic variation in the intensity of antagonistic interactions have had only minor modifying effects on the evolutionary trajectories of floral advertisement in plant populations in this system. Thus, pollinator-driven floral trait evolution in D. scandens in the study area appears not to be influenced by conflicting seed-predator-mediated selection

Intersexual conflict over seed size is stronger in more outcrossed populations of a mixed-mating plant

In polyandrous species, fathers benefit from attracting greater maternal investment toward their offspring at the expense of the offspring of other males, while mothers should usually allocate resources equally among offspring. This conflict can lead to an evolutionary arms race between the sexes, manifested through antagonistic genes whose expression in offspring depends upon the parent of origin. The arms race may involve an increase in the strength of maternally versus paternally derived alleles engaged in a “tug of war” over maternal provisioning or repeated “recognition-avoidance” coevolution where growth-enhancing paternally derived alleles evolve to escape recognition by maternal genes targeted to suppress their effect. Here, we develop predictions to distinguish between these two mechanisms when considering crosses among populations that have reached different equilibria in this intersexual arms race. We test these predictions using crosses within and among populations of Dalechampia scandens (Euphorbiaceae) that presumably have experienced different intensities of intersexual conflict, as inferred from their historical differences in mating system. In crosses where the paternal population was more outcrossed than the maternal population, hybrid seeds were larger than those normally produced in the maternal population, whereas when the maternal population was more outcrossed, hybrid seeds were smaller than normal. These results confirm the importance of mating systems in determining the intensity of intersexual conflict over maternal investment and provide strong support for a tug-of-war mechanism operating in this conflict. They also yield clear predictions for the fitness consequences of gene flow among populations with different mating histories.acceptedVersion© 2018. This is the authors' accepted and refereed manuscript to the article. The final authenticated version is available online at: https://doi.org/10.1073/pnas.181097911

Growth and Asymmetry of Soil Microfungal Colonies from “Evolution Canyon,” Lower Nahal Oren, Mount Carmel, Israel

Fluctuating asymmetry is a contentious indicator of stress in populations of animals and plants. Nevertheless, it is a measure of developmental noise, typically obtained by measuring asymmetry across an individual organism's left-right axis of symmetry. These individual, signed asymmetries are symmetrically distributed around a mean of zero. Fluctuating asymmetry, however, has rarely been studied in microorganisms, and never in fungi.We examined colony growth and random phenotypic variation of five soil microfungal species isolated from the opposing slopes of “Evolution Canyon,” Mount Carmel, Israel. This canyon provides an opportunity to study diverse taxa inhabiting a single microsite, under different kinds and intensities of abiotic and biotic stress. The south-facing “African” slope of “Evolution Canyon” is xeric, warm, and tropical. It is only 200 m, on average, from the north-facing “European” slope, which is mesic, cool, and temperate. Five fungal species inhabiting both the south-facing “African” slope, and the north-facing “European” slope of the canyon were grown under controlled laboratory conditions, where we measured the fluctuating radial asymmetry and sizes of their colonies. from the “African” slope were more asymmetric than those from the “European” slope.Our study suggests that fluctuating radial asymmetry has potential as an indicator of random phenotypic variation and stress in soil microfungi. Interaction of slope and species for both growth rate and asymmetry of microfungi in a common environment is evidence of genetic differences between the “African” and “European” slopes of “Evolution Canyon.

Within-individual phenotypic plasticity in flowers fosters pollination niche shift

Authors thank Raquel Sánchez, Angel Caravante, Isabel Sánchez Almazo, Tatiana López Pérez, Samuel Cantarero, María José Jorquera and Germán Fernández for helping us during several phases of the study and Iván Rodríguez Arós for drawing the insect silhouettes. This research is supported by grants from the Spanish Ministry of Science, Innovation and Universities (CGL2015-71634-P, CGL2015-63827-P, CGL2017-86626-C2-1-P, CGL2017- 86626-C2-2-P, UNGR15-CE-3315, including EU FEDER funds), Junta de Andalucía (P18- FR-3641), Xunta de Galicia (CITACA), BBVA Foundation (PR17_ECO_0021), and a contract grant to C.A. from the former Spanish Ministry of Economy and Competitiveness (RYC-2012-12277). This is a contribution to the Research Unit Modeling Nature, funded by the Consejería de Economía, Conocimiento, Empresas y Universidad, and European Regional Development Fund (ERDF), reference SOMM17/6109/UGR.Phenotypic plasticity, the ability of a genotype of producing different phenotypes when exposed to different environments, may impact ecological interactions. We study here how within-individual plasticity in Moricandia arvensis flowers modifies its pollination niche. During spring, this plant produces large, cross-shaped, UV-reflecting lilac flowers attracting mostly long-tongued large bees. However, unlike most co-occurring species, M. arvensis keeps flowering during the hot, dry summer due to its plasticity in key vegetative traits. Changes in temperature and photoperiod in summer trigger changes in gene expression and the production of small, rounded, UV-absorbing white flowers that attract a different assemblage of generalist pollinators. This shift in pollination niche potentially allows successful reproduction in harsh conditions, facilitating M. arvensis to face anthropogenic perturbations and climate change. Floral phenotypes impact interactions between plants and pollinators. Here, the authors show that Moricandia arvensis displays discrete seasonal plasticity in floral phenotype, with large, lilac flowers attracting long-tongued bees in spring and small, rounded, white flowers attracting generalist pollinators in summer.Spanish Ministry of Science, Innovation and Universities (EU FEDER funds) CGL2015-71634-P CGL2015-63827-P CGL2017-86626-C2-1-P CGL2017-86626-C2-2-P UNGR15-CE-3315Junta de Andalucia P18-FR-3641Xunta de GaliciaBBVA Foundation PR17_ECO_0021Spanish Ministry of Economy and Competitiveness RYC-2012-12277Consejeria de Economia, Conocimiento, Empresas y Universidad SOMM17/6109/UGREuropean Union (EU) SOMM17/6109/UG