How to be a dioecious fig: Chemical mimicry between sexes matters only when both sexes flower synchronously.

In nursery pollination mutualisms, which are usually obligate interactions, olfactory attraction of pollinators by floral volatile organic compounds (VOCs) is the main step in guaranteeing partner encounter. However, mechanisms ensuring the evolutionary stability of dioecious fig-pollinator mutualisms, in which female fig trees engage in pollination by deceit resulting in zero reproductive success of pollinators that visit them, are poorly understood. In dioecious figs, individuals of each sex should be selected to produce odours that their pollinating wasps cannot distinguish, especially since pollinators have usually only one choice of a nursery during their lifetime. To test the hypothesis of intersexual chemical mimicry, VOCs emitted by pollen-receptive figs of seven dioecious species were compared using headspace collection and gas chromatography-mass spectrometry analysis. First, fig-flower scents varied significantly among species, allowing host-species recognition. Second, in species in which male and female figs are synchronous, intersexual VOC variation was not significant. However, in species where figs of both sexes flower asynchronously, intersexual variation of VOCs was detectable. Finally, with one exception, there was no sexual dimorphism in scent quantity. We show that there are two ways to use scent to be a dioecious fig based on differences in flowering synchrony between the sexes.

Floral volatiles, pollinator sharing and diversification in the fig-wasp mutualism: insights from Ficus natalensis, and its two wasp pollinators (South Africa).

Combining biogeographic, ecological, morphological, molecular and chemical data, we document departure from strict specialization in the fig-pollinating wasp mutualism. We show that the pollinating wasps Elisabethiella stuckenbergi and Elisabethiella socotrensis form a species complex of five lineages in East and Southern Africa. Up to two morphologically distinct lineages were found to co-occur locally in the southern African region. Wasps belonging to a single lineage were frequently the main regional pollinators of several Ficus species. In South Africa, two sister lineages, E. stuckenbergi and E. socotrensis, pollinate Ficus natalensis but only E. stuckenbergi also regularly pollinates Ficus burkei. The two wasp species co-occur in individual trees of F. natalensis throughout KwaZulu-Natal. Floral volatile blends emitted by F. natalensis in KwaZulu-Natal were similar to those emitted by F. burkei and different from those produced by other African Ficus species. The fig odour similarity suggests evolutionary convergence to attract particular wasp species. The observed pattern may result from selection for pollinator sharing among Ficus species. Such a process, with one wasp species regionally pollinating several hosts, but several wasp species pollinating a given Ficus species across its geographical range could play an important role in the evolutionary dynamics of the Ficus-pollinating wasp association.

Ficus racemosa is pollinated by a single population of a single agaonid wasp species in continental South-East Asia.

High specificity in the Ficus-agaonid wasp mutualism has lead to the assumption of a mostly 'one-to-one' relationship, albeit with some exceptions. This view has been challenged by new molecular data in recent years, but surprisingly little is known about local and spatial genetic structuring of agaonid wasp populations. Using microsatellite markers, we analysed genetic structuring of Ceratosolen fusciceps, the fig wasp pollinating Ficus racemosa, a fig tree species widely distributed from India to Australia. In sampling stretching from the south of China to the south of Thailand we found evidence for only a single pollinating wasp species in continental South-East Asian mainland. We found no evidence for the co-occurrence of cryptic species within our subcontinent sampling zone. We observed no spatial genetic structure within sites and only limited structuring over the whole sampling zone, suggesting that F. racemosa is pollinated by a single population of a single agaonid wasp species all over continental South-East Asia. An additional sample of wasps collected on F. racemosa in Australia showed clear-cut genetic differentiation from the Asian continent, suggesting allopatric divergence into subspecies or species. We propose that the frequent local co-occurrence of sister species found in the literature mainly stems from contact zones between biogeographic regions, and that a single pollinator species over wide areas might be the more common situation everywhere else.

Isolation and characterization of microsatellite primers for Ceratosolen fusciceps, the fig-pollinating wasp of Ficus racemosa, and amplification in two populations.

Ten microsatellite loci were isolated and characterized for Ceratosolen fusciceps, the pollinating wasp of Ficus racemosa, based on individuals from Xishuangbanna (China) and Chiangmai (Thailand). High levels of variation were found among loci for both populations; allelic number varied from two to 18 (respectively from two to 22), expected heterozygosities ranged from 0.362 to 0.890 (respectively from 0.430 to 0.930).

Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx).

Inbreeding depression reflects the negative consequences of increased homozygosity at genes that affect fitness. We investigate inbreeding depression in a semi-free-ranging colony of mandrills (Mandrillus sphinx), using high-quality pedigree data, comprising five maternal generations and 20 years of morphological and demographic data. We examine the relationship between inbreeding coefficients and four fitness correlates: two growth parameters (mass and height for age) and longevity in both sexes, and age at first conception in females. Inbreeding was correlated with both growth parameters, but only in females, with inbred females being smaller than noninbred females. Inbreeding was also correlated significantly with age at first conception, with inbred females giving birth earlier in life than noninbred females. We suggest that sex-biased maternal investment may explain this sex-differential response to inbreeding, although the lack of a significant association between inbreeding and growth in males may also be due to the provisioned nature of the colony. The surprising relationship between age at first conception and inbreeding may be related to smaller adult size in inbred females, or to their being less able to escape from male sexual coercion.

Parallels in the evolution of the two largest New and Old World seed-beetle genera (Coleoptera, Bruchidae).

This study provides the first phylogenetic analysis of a large sample of the two largest genera of seed-beetles, Acanthoscelides Schilsky and Bruchidius Schilsky, which mostly feed on legumes (Fabaceae). The goal of this study was to investigate evolutionary patterns in relation to biogeography and host-plant associations. We used three mitochondrial molecular markers and parsimony and Bayesian inference methods to reconstruct the phylogeny of 76 species. In addition, we critically reviewed host-plant records in the literature for these two bruchid genera. Our results demonstrated the existence of two major clades, one New World and one largely Old World, which generally correspond to the two genera. Yet, current classification of several species is erroneous, so that both genera as currently defined are paraphyletic. We highlighted a strong trend toward specialization (with high taxonomic conservatism in host-plant use) exhibited by the two studied genera. However, we showed the existence of several host shifts during the evolution of this group of bruchids. Our phylogenetic hypotheses and our evaluation of host-plant associations both suggest that the two genera have undergone parallel evolution, as they have independently colonized similar host plants in their respective areas of distribution. Our estimation of divergence times indicated a more ancient origin for bruchids than that suggested by the fossil records. Interestingly, the suggested timing of diversification is consistent with the hypothesis of a radiation that could have occurred contemporaneously with the diversification of their legume hosts.

Genetic diversity and reproductive success in mandrills (Mandrillus sphinx).

Recent studies of wild animal populations have shown that estimators of neutral genetic diversity, such as mean heterozygosity, are often correlated with various fitness traits, such as survival, disease susceptibility, or reproductive success. We used two estimators of genetic diversity to explore the relationship between heterozygosity and reproductive success in male and female mandrills (Mandrillus sphinx) living in a semifree ranging setting in Gabon. Because social rank is known to influence reproductive success in both sexes, we also examined the correlation between genetic diversity and social rank in females, and acquisition of alpha status in males, as well as length of alpha male tenure. We found that heterozygous individuals showed greater reproductive success, with both females and males producing more offspring. However, heterozygosity influenced reproductive success only in dominant males, not in subordinates. Neither the acquisition of alpha status in males, nor social rank in females, was significantly correlated with heterozygosity, although more heterozygous alpha males showed longer tenure than homozygous ones. We also tested whether the benefits of greater genetic diversity were due mainly to a genome-wide effect of inbreeding depression or to heterosis at one or a few loci. Multilocus effects best explained the correlation between heterozygosity and reproductive success and tenure, indicating the occurrence of inbreeding depression in this mandrill colony.

Self-pollination and its costs in a monoecious fig (Ficus aurea, Moraceae) in a highly seasonal subtropical environment.

The unusual floral phenology of most monoecious figs, related to their highly specialized pollination mutualism with agaonid wasps, combines pronounced dichogamy at the level of inflorescences and individuals with population-level asynchrony in flowering. This floral phenology ensures that outcrossing strongly predominates. Fig populations may thus be expected to possess deleterious recessive alleles that lead to inbreeding depression when selfing does occur. However, whether monoecious figs are self-compatible and whether selfing results in inbreeding depression have never been investigated. Using wasps as "pollination tools" and exploiting infrequent overlap in male and female phases on the same tree, we conducted controlled selfed and outcrossed pollination experiments in Ficus aurea. Our results show that this species is totally self-compatible. No negative effects of selfing could be demonstrated on syconium retention, number of vacant ovaries, seed set, or seed germination. However, wasp production had a tendency to be higher after self-pollination. While it is possible that inbreeding depression is expressed at later developmental stages, its absence at the early stages we examined is nonetheless surprising for a plant expected to be highly outcrossed. It is likely that selection pressures other than avoidance of inbreeding are responsible for the evolution and maintenance of the unusual floral phenology of figs.

Carbon allocation to volatiles and other reproductive components in male Ficus carica (Moraceae).

Volatile compounds are often mediators of plant-pollinator interactions. Their emission is presumed to be costly, but this cost has seldom been quantified. Figs of Ficus carica (a dioecious species) release volatile compounds when receptive, thus attracting the agaonid wasp Blastophaga psenes. In dioecious fig species, wasps lay eggs inside male figs and pollinate female ones. For a male tree, we estimated carbon allocation to reproduction using the annual growth module (AGM) as the unit of measurement. Over the growing season, leaf and fig carbon exchange and construction costs were measured, as well as carbon investment in stamens, provisioning pollinators, and biosynthesis and release of volatile compounds. Representativity of the tree studied was evaluated by measuring some of these parameters on seven other male fig trees. The results show that 7.6-16.4% of the carbon assimilated by leaves and figs was invested in reproduction. Of the carbon invested in reproduction, pollinator attraction and feeding represented only 0.08-0.12% and 1.84-2.33%, respectively, while pollinator sheltering (fig construction and respiration) represented 97.6-98.0%. In this strict and coevolved plant-pollinator association, the main male reproductive investment was thus in the structures sheltering the associated pollinators.

Evidence for a switch in the reproductive biology of Rubus alceifolius (Rosaceae) towards apomixis, between its native range and its area of introduction.

We compared the reproductive system of Rubus alceifolius in its native range in Southeast Asia, in Madagascar, where the plant was introduced apparently some centuries ago, and in La Réunion, an Indian Ocean island onto which R. alceifolius was introduced (from Madagascan source populations) around 1850. While tetraploidy makes it impossible to analyze variation in R. alceifolius using classical methods of population genetics, both the patterns of genetic diversity (as revealed by AFLP [amplified fragment length polymorphism] markers) and differences between half-sib progeny and their maternal parents (revealed by microsatellite markers) show that in the plant's native range in southeast Asia, seeds are produced sexually. In contrast, in Madagascar sexual reproduction cannot alone account for the genetic patterns observed with microsatellite markers. Over 85% of the half-sib progeny resulting from open pollination gave multilocus genotypes identical to those of their respective maternal parents, despite the fact that the latter had alleles that were rare in the population. The other progeny differed in having an allele with one motif more or less than that of the maternal parent. Seeds thus appear to be produced mostly or exclusively by apomixis in Madagascar. We present findings suggesting that Madagascan populations result from hybridization of introduced R. alceifolius and native populations of R. roridus, a closely related species of Rubus subgenus Malachobatus, and suggest that apomixis was a consequence of this hybridization. In Reunionese populations of R. alceifolius (derived from Madagascan populations), seeds obtained in controlled pollination experiments were all genetically identical to maternal parents. While genetic variation (microsatellite markers) in Reunionese populations was low, it was sufficient to allow us to demonstrate that seeds could not have resulted from fertilization by the pollen donors chosen for controlled pollinations, or from autogamy, and were produced exclusively by apomixis.

Comparison of genetic diversity of the invasive weed Rubus alceifolius poir. (Rosaceae) in its native range and in areas of introduction, using amplified fragment length polymorphism (AFLP) markers.

Theory predicts that colonization of new areas will be associated with population bottlenecks that reduce within-population genetic diversity and increase genetic differentiation among populations. This should be especially true for weedy plant species, which are often characterized by self-compatible breeding systems and vegetative propagation. To test this prediction, and to evaluate alternative scenarios for the history of introduction, the genetic diversity of Rubus alceifolius was studied with amplified fragment length polymorphism (AFLP) markers in its native range in southeast Asia and in several areas where this plant has been introduced and is now a serious weed (Indian Ocean islands, Australia). In its native range, R. alceifolius showed great genetic variability within populations and among geographically close populations (populations sampled ranging from northern Vietnam to Java). In Madagascar, genetic variability was somewhat lower than in its native range, but still considerable. Each population sampled in the other Indian Ocean islands (Mayotte, La Réunion, Mauritius) was characterized by a single different genotype of R. alceifolius for the markers studied, and closely related to individuals from Madagascar. Queensland populations also included only a single genotype, identical to that found in Mauritius. These results suggest that R. alceifolius was first introduced into Madagascar, perhaps on multiple occasions, and that Madagascan individuals were the immediate source of plants that colonized other areas of introduction. Successive nested founder events appear to have resulted in cumulative reduction in genetic diversity. Possible explanations for the monoclonality of R. alceifolius in many areas of introduction are discussed.

Figs and fig pollinators: evolutionary conflicts in a coevoled mutualism.

Figs and fig wasps form one of the best known examples of species-specific mutualism and coevolution. Recent experiments and observations have led to a better understanding of the evolutionary processes involved in the origin and maintenance of species interactions. The observed fine-tuned traits involve not only coevolution but also selection acting on only one of the partners. Furthermore, some of the 'fine-tuned traits' appear to be be preadaptions - traits that existed before the mutalism was establised.