Managed honeybees decrease pollination limitation in self-compatible but not in self-incompatible crops.

Modern agriculture is becoming increasingly pollinator-dependent. However, the global stock of domesticated honeybees is growing at a slower rate than its demand, while wild bees are declining worldwide. This uneven scenario of high pollinator demand and low pollinator availability can translate into increasing pollination limitation, reducing the yield of pollinator-dependent crops. However, overall assessments of crop pollination limitation and the factors determining its magnitude are missing. Based on 52 published studies including 30 crops, we conducted a meta-analysis comparing crop yield in pollen-supplemented versus open-pollinated flowers. We assessed the overall magnitude of pollination limitation and whether this magnitude was influenced by (i) the presence/absence of managed honeybees, (ii) crop compatibility system (i.e. self-compatible/self-incompatible) and (iii) the interaction between these two factors. Overall, pollen supplementation increased yield by approximately 34%, indicating sizable pollination limitation. Deployment of managed honeybees and self-compatibility were associated with lower pollination limitation. Particularly, active honeybee management decreased pollination limitation among self-compatible but apparently not among self-incompatible crops. These findings indicate that current pollination regimes are, in general, inadequate to maximize crop yield, even when including managed honeybees, and stress the need of transforming the pollination management paradigm of agricultural landscapes.

Intentional and unintentional selection during plant domestication: herbivore damage, plant defensive traits and nutritional quality of fruit and seed crops.

Greater susceptibility to herbivory can arise as an effect of crop domestication. One proposed explanation is that defenses decreased intentionally or unintentionally during the domestication process, but evidence for this remains elusive. An alternative but nonexclusive explanation is presumed selection for higher nutritional quality. We used a metaanalytical approach to examine susceptibility to herbivores in fruit and seed crops and their wild relatives. Our analyses provide novel insights into the mechanisms of increased susceptibility by evaluating whether it can be attributed to either a reduction in herbivore defensive traits, including direct/indirect and constitutive/inducible defenses, or an increase in the nutritional content of crops. The results confirm higher herbivory and lower levels of all types of defenses in crops compared to wild relatives, although indirect defenses were more affected than direct ones. Contrary to expectations, nutritional quality was lower in crops than in wild relatives, which may enhance biomass loss to herbivores if they increase consumption to meet nutritional requirements. Our findings represent an important advance in our understanding of how changes in defensive and nutritional traits following domestication could influence, in combination or individually, crop susceptibility to herbivore attacks.

An overlooked plant-parakeet mutualism counteracts human overharvesting on an endangered tree.

The exponential growth of the human population often causes the overexploitation of resources and disruption of ecological interactions. Here, we propose that the antagonist effect of humans on exploited species might be alleviated with the advent of a second predator species. We focused on the complex interactions between an endangered conifer (Araucaria araucana) and two seed exploiters: the Austral parakeet (Enicognathus ferrugineus) and human seed collectors. We tested the importance of partial seed consumption by parakeets as an escape from human seed harvesting. Although parakeets frequently ate whole seeds, a substantial proportion of the seeds found under trees were only partially eaten and avoided by human seed collectors. These seeds germinated at a similar proportion but faster than intact seeds under laboratory conditions. Our results revealed an overlooked mutualism between parakeets and an endangered tree. Incomplete seed eating by parakeets, plus selection against these eaten seeds by humans, may enhance regeneration possibilities for this conifer species subject to human seed collection, turning the scale of the antagonism-mutualism continuum to the mutualistic side. In this context, parakeets might be providing an important service in those forests subject to human harvesting by allowing a fraction of seeds to escape human predation.

Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence.

Conservation biology can profit greatly from incorporating a phylogenetic perspective into analyses of patterns and drivers of species extinction risk. We applied such an approach to analyse patterns of bumblebee (Bombus) decline. We assembled a database representing approximately 43% of the circa 260 globally known species, which included species extinction risk assessments following the International Union fo Conservation of Nature Red List categories and criteria, and information on species traits presumably associated with bumblebee decline. We quantified the strength of phylogenetic signal in decline, range size, tongue length and parasite presence. Overall, about one-third of the assessed bumblebees are declining and declining species are not randomly distributed across the Bombus phylogeny. Susceptible species were over-represented in the subgenus Thoracobombus (approx. 64%) and under-represented in the subgenus Pyrobombus (approx. 6%). Phylogenetic logistic regressions revealed that species with small geographical ranges and those in which none of three internal parasites were reported (i.e. Crithidia bombi, Nosema spp. or Locustacarus buchneri) were particularly vulnerable. Bumblebee evolutionary history will be deeply eroded if most species from threatened clades, particularly those stemming from basal nodes, become finally extinct. The habitat of species with restricted distribution should be protected and the importance of pathogen tolerance/resistance as mechanisms to deal with pathogens needs urgent research.

The phylogenetic structure of plant-pollinator networks increases with habitat size and isolation.

Similarity among species in traits related to ecological interactions is frequently associated with common ancestry. Thus, closely related species usually interact with ecologically similar partners, which can be reinforced by diverse co-evolutionary processes. The effect of habitat fragmentation on the phylogenetic signal in interspecific interactions and correspondence between plant and animal phylogenies is, however, unknown. Here, we address to what extent phylogenetic signal and co-phylogenetic congruence of plant-animal interactions depend on habitat size and isolation by analysing the phylogenetic structure of 12 pollination webs from isolated Pampean hills. Phylogenetic signal in interspecific interactions differed among webs, being stronger for flower-visiting insects than plants. Phylogenetic signal and overall co-phylogenetic congruence increased independently with hill size and isolation. We propose that habitat fragmentation would erode the phylogenetic structure of interaction webs. A decrease in phylogenetic signal and co-phylogenetic correspondence in plant-pollinator interactions could be associated with less reliable mutualism and erratic co-evolutionary change.

The effects of inbreeding, genetic dissimilarity and phenotype on male reproductive success in a dioecious plant.

Pollen fate can strongly affect the genetic structure of populations with restricted gene flow and significant inbreeding risk. We established an experimental population of inbred and outbred Silene latifolia plants to evaluate the effects of (i) inbreeding depression, (ii) phenotypic variation and (iii) relatedness between mates on male fitness under natural pollination. Paternity analysis revealed that outbred males sired significantly more offspring than inbred males. Independently of the effects of inbreeding, male fitness depended on several male traits, including a sexually dimorphic (flower number) and a gametophytic trait (in vitro pollen germination rate). In addition, full-sib matings were less frequent than randomly expected. Thus, inbreeding, phenotype and genetic dissimilarity simultaneously affect male fitness in this animal-pollinated plant. While inbreeding depression might threaten population persistence, the deficiency of effective matings between sibs and the higher fitness of outbred males will reduce its occurrence and counter genetic erosion.

Comparative population genetic structure in a plant-pollinator/seed predator system.

Comparative analyses of spatial genetic structure of populations of plants and the insects they interact with provide an indication of how gene flow, natural selection and genetic drift may jointly influence the distribution of genetic variation and potential for local co-adaptation for interacting species. Here, we analysed the spatial scale of genetic structure within and among nine populations of an interacting species pair, the white campion Silene latifolia and the moth Hadena bicruris, along a latitudinal gradient across Northern/Central Europe. This dioecious, short-lived perennial plant inhabits patchy, often disturbed environments. The moth H. bicruris acts both as its pollinator and specialist seed predator that reproduces by laying eggs in S. latifolia flowers. We used nine microsatellite markers for S. latifolia and eight newly developed markers for H. bicruris. We found high levels of inbreeding in most populations of both plant and pollinator/seed predator. Among populations, significant genetic structure was observed for S. latifolia but not for its pollinator/seed predator, suggesting that despite migration among populations of H. bicruris, pollen is not, or only rarely, carried over between populations, thus maintaining genetic structure among plant populations. There was a weak positive correlation between genetic distances of S. latifolia and H. bicruris. These results indicate that while significant structure of S. latifolia populations creates the potential for differentiation at traits relevant for the interaction with the pollinator/seed predator, substantial gene flow in H. bicruris may counteract this process in at least some populations.

Disassortative mating, sexual specialization, and the evolution of gender dimorphism in heterodichogamous Acer opalus.

In sexually polymorphic species, the morphs are maintained by frequency-dependent selection through disassortative mating. In heterodichogamous populations in which disassortative mating occurs between the protandrous and protogynous morphs, a decrease in female fitness in one morph is hypothesized to drive sexual specialization in the other morph, resulting in dimorphic populations. We test these ideas in a population of the heterodichogamous species, Acer opalus. We assessed both prospective gender of individuals in terms of their allocations and actual parentage using microsatellites; we found that most matings in A. opalus occur disassortatively. We demonstrate that the protogynous morph is maintained by frequency-dependent selection, but that maintenance of males versus protandrous individuals depends on their relative siring success, which changes yearly. Seeds produced later in the reproductive season were smaller than those produced earlier; this should compromise reproduction through ovules in protandrous individuals, rendering them male biased in gender. Time-dependent gender and paternity analyses indicate that the sexual morphs are specialized in their earlier sexual functions, mediated by the seasonal decrease in seed size. Our results confirm that mating patterns are context-dependent and change seasonally, suggesting that sexual specialization can be driven by seasonal effects on fitness gained through one of the two sexual functions.

Siring success and paternal effects in heterodichogamous Acer opalus.

BACKGROUND AND AIMS: Heterodichogamy (a dimorphic breeding system comprising protandrous and protogynous individuals) is a potential starting point in the evolution of dioecy from hermaphroditism. In the genus Acer, previous work suggests that dioecy evolved from heterodichogamy through an initial spread of unisexual males. Here, the question is asked as to whether the different morphs in Acer opalus, a species in which males co-exist with heterodichogamous hermaphrodites, differ in various components of male in fitness. METHODS: Several components of male fertility were analysed. Pollination rates in the male phase were recorded across one flowering period. Pollen viability was compared among morphs through hand pollinations both with pollen from a single sexual morph and also simulating a situation of pollen competition; in the latter experiment, paternity was assessed with microsatellite markers. It was also determined whether effects of genetic relatedness between pollen donors and recipients could influence the siring success. Finally, paternal effects occurring beyond the fertilization process were tested for by measuring the height reached by seedlings with different sires over three consecutive growing seasons. KEY RESULTS: The males and protandrous morphs had higher pollination rates than the protogynous morph, and the seedlings they sired grew taller. No differences in male fertility were found between males and protandrous individuals. Departures from random mating due to effects of genetic relatedness among sires and pollen recipients were also ruled out. CONCLUSIONS: Males and protandrous individuals are probably better sires than protogynous individuals, as shown by the higher pollination rates and the differential growth of the seedlings sired by these morphs. In contrast, the fertility of males was not higher than the male fertility of the protandrous morph. While the appearance of males in sexually specialized heterodichogamous populations is possible, even in the absence of a fitness advantage, it is not clear that males can be maintained at an evolutionary equilibrium with two classes of heterodichogamous hermaphrodites.

Adaptive evolution of reproductive and vegetative traits driven by breeding systems.

The evolution of inflorescence size, a key trait in reproductive success, was studied in the genus Acer under a perspective of adaptive evolution. Breeding systems, hypothesized to indicate different levels of mating competition, were considered as the selective scenarios defining different optima of inflorescence size. Larger inflorescences, which increase male fitness by generating larger floral displays, were hypothesized to be selected under scenarios with higher competition with unisexuals. An identical approach was used to test if the same selective regimes could be driving the evolution of leaf size, a vegetative trait that was found to be correlated with inflorescence size. A Brownian motion model of inflorescence/leaf-size evolution (which cannot distinguish between changes caused by pure drift processes and changes caused by natural selection in rapidly and randomly changing environments) was compared with several adaptive Ornstein-Uhlenbeck (OU) models, which can quantify the effects of both stochasticity and natural selection. The best-fitting model for inflorescence/leaf-size evolution was an OU model with three optima that increased with the level of mating competition. Both traits evolved under the same selective regimes and in the same direction, confirming a pattern of correlated evolution. These results show that a selective regime hypothetically related to the evolution of a reproductive trait can also explain the evolution of a vegetative trait.

Repeated evolution of dioecy from androdioecy in Acer.

The evolution of breeding systems was studied in the genus Acer, with special attention to the origin of androdioecy and dioecy, using a phylogenetic approach. Parsimony and maximum-likelihood techniques were used to infer the ancestral character state and trends in the evolution of breeding systems. Information on breeding systems was obtained from the literature, and phylogenetic relationships were taken from three published phylogenies. Although a general trend from duodichogamy to dioecy through heterodichogamy has been proposed for the genus Acer, our results show that a general trend is not detected when phylogenetic relationships are taken into account. Dioecy appeared as a derived state that evolved at least three times and never reversed towards other states. Three different paths to dioecy have been followed in the genus Acer: from heterodichogamous androdioecy; from heterodichogamous trioecy; and from dichogamous subdioecy. Therefore, although the best documented cases of evolution of androdioecy indicate that this breeding system evolves from dioecy, in the genus Acer the opposite situation occurs (androdioecy leading to dioecy). Here we discuss the role of inbreeding avoidance and sexual specialization as selective forces driving the evolution of dioecy in the genus Acer.