Sexual selection on population-level mating opportunities drives morph ratios in a fig wasp with extreme male dimorphism

Background: Alternative mating tactics are widespread in animals and associated with extreme morphological polymorphism in some insects. Some fig wasps have both highly modified wingless males and dispersing winged males. Wingless males mate inside figs before females disperse, while winged males mate elsewhere after dispersal. Hamilton proposed a model for this system with morphs determined by alternative alleles. This has an equilibrium where the proportion of winged males equals the proportion of females dispersing unmated; i.e. the proportion of matings that they obtain. Previously, we have shown qualitative support for this prediction across nine wing-dimorphic fig wasp species. Here I test the quantitative prediction in the fig wasp Pseudidarnes minerva. In addition, some fig wasp species that lack winged males, but have two wingless morphs, show a conditional strategy with morph determination influenced by the number of wasps developing in a patch. I also test for this alternative pattern in the wing-dimorphic P. minerva. Results: I sampled 114 figs that contained a mean of 2.1 P. minerva wasps from 44 trees across four sites in Sydney, Australia. At the whole population level, the proportion of winged males (0.84 or 0.79 corrected for sampling bias) did not differ significantly from the proportion of unmated females (0.84), providing strong quantitative support for the prediction of Hamilton’s model. In addition, there was no evidence for other factors, such as local mate competition or fighting between wingless males, that could violate simplifying assumptions of the model. Meanwhile, the proportion of winged males was not correlated with the number of wasps per fig, providing no evidence for a conditional strategy. Conclusion: The morph ratio in P. minerva is consistent with Hamilton’s simple Mendelian strategy model, where morph ratios are set by average mating opportunities at the population level. This contrasts with some fig wasps from another subfamily that show conditional morph determination, allowing finer scale adaptation to fig-level mating opportunities. However, these conditional cases do not involve wing polymorphism. Male polymorphism is common and variable in fig wasps and has evolved independently in multiple lineages with apparently different underlying mechanisms

Sex and flowers: testing the resource-dependent selection hypothesis for flower sex allocation

Context: Monoecious plants can adjust their proportional investment in male and female flowers to maximise reproductive fitness. The female reproductive function (seeds) often has greater resource costs than the male (pollen). Larger plants are generally thought to have greater resource availability and should have a female biased sex ratio, referred to as the size-dependent selection hypothesis. However, empirical tests of this hypothesis have found mixed support. This may be because size alone is not always a reliable proximate value for resource availability, which can be influenced by other abiotic factors. Aims: Breynia oblongifolia (Phyllanthaceae) is a perennial monoecious plant with unisexual moth-pollinated flowers from eastern Australia. Fruit production in Breynia is heavily influenced by rainfall, which is highly variable. We hypothesised that where soil moisture limits female function, Breynia would produce more male flowers (i.e. resource-dependent selection). Methods: We used a multi-year observational dataset to look for evidence of resource-dependent flower sex ratios in a wild population and conducted a manipulative glasshouse experiment to test alternative hypotheses for flower sex selection. Key results: In both our manipulative glasshouse experiment and observed wild population, decreasing soil water content resulted in higher proportions of male flowers, supporting the resource-dependent sex selection hypothesis. Conclusions: Soil moisture influences flower sex ratios but plant size does not. Implications: Future studies should not assume that height equates to resource wealth, as this is often overly simplistic and ignores the potential for key resources, like soil moisture or light, to fluctuate

Fishing for flies : testing the efficacy of "stink stations" for promoting blow flies as pollinators in mango orchards

Pollinator communities are composed of diverse groups of insects, with radically different life histories and resource needs. Blow flies are known to visit a variety of economically important crop plants. Larval blow flies develop by feeding on decaying animals. Some fruit growers are known to place carrion on farms during the flowering season to attract adult blow flies (Calliphoridae). However, the efficacy of these “stink stations” has not been tested. We conducted a series of experiments to determine: 1) if stink stations promote the abundance of blow flies in mango orchards (Mangifera indica L.), 2) if any increases in the abundance of flies acts to promote pollination and fruit set in Australian mango orchards. Farms with stink stations had approximately three times more flies than control farms. However, the increased abundance of blow flies did not result in increased fruit set. Although stink stations increased the abundance of blow flies, we found no evidence that their use improves mango yield. This may be due to pollination saturation by a highly abundant native hover fly, Mesembrius bengalensis (Syrphidae), during our study. We hypothesize that stink stations may only be beneficial in years or regions where other pollinators are less abundant

Staying in touch : how highly specialised moth pollinators track host plant phenology in unpredictable climates

Background: For specialised pollinators, the synchrony of plant and pollinator life history is critical to the persistence of pollinator populations. This is even more critical in nursery pollination, where pollinators are obligately dependant on female host plant flowers for oviposition sites. Epicephala moths (Gracillariidae) form highly specialised nursery pollination mutualisms with Phyllanthaceae plants. Several hundred Phyllanthaceae are estimated to be exclusively pollinated by highly specific Epicephala moths, making these mutualisms an outstanding example of plant–insect coevolution. However, there have been no studies of how Epicephala moths synchronise their activity with host plant flowering or persist through periods when flowers are absent. Such knowledge is critical to understanding the ecology and evolutionary stability of these mutualisms. We surveyed multiple populations of both Breynia oblongifolia (Phyllanthaceae) and it’s Epicephala pollinators for over two years to determine their phenology and modelled the environmental factors that underpin their interactions. Results: The abundance of flowers and fruits was highly variable and strongly linked to local rainfall and photoperiod. Unlike male flowers and fruits, female flowers were present throughout the entire year, including winter. Fruit abundance was a significant predictor of adult Epicephala activity, suggesting that eggs or early instar larvae diapause within dormant female flowers and emerge as fruits mature. Searches of overwintering female flowers confirmed that many contained pollen and diapausing pollinators. We also observed diapause in Epicephala prior to pupation, finding that 12% (9/78) of larvae emerging from fruits in the autumn entered an extended diapause for 38–48 weeks. The remaining autumn emerging larvae pupated directly without diapause, suggesting a possible bet-hedging strategy. Conclusions: Epicephala appear to use diapause at multiple stages in their lifecycle to survive variable host plant phenology. Furthermore, moth abundance was predicted by the same environmental variables as male flowers, suggesting that moths track flowering through temperature. These adaptations may thereby mitigate against unpredictability in the timing of fruiting and flowering because of variable rainfall. It remains to be seen how widespread egg diapause and pre-pupal diapause may be within Epicephala moths, and, furthermore, to what degree these traits may have facilitated the evolution of these highly diverse mutualisms

Habitat complexity affects functional traits and diversity of ant assemblages in urban green spaces (Hymenoptera: Formicidae)

Habitat complexity conferred by vegetation characteristics mediates key processes that govern the assemblage of insect communities. Thus, species within the community should only persist if their functional traits are well-matched to the conditions of their environment. Here, we compared ant assemblages between habitats in terms of species richness and functional-trait distribution at the species and the assemblage level. Ants were collected from 36 sites representing different degrees of habitat complexity mediated by standing vegetation. We found fewer ant species in simpler habitats, supporting the "habitat-heterogeneity" hypothesis. We measured key functional traits of ants that reflect their foraging and dispersal strategies, such as body size, femur length, antenna scape length, and head length / width. Interactions of species traits with measured habitat complexity variables were assessed at the species and the assemblage level using a fourth-corner approach. Ant traits were closely related to environmental complexity. In wooded habitats, ants were larger and had broader heads, while ants with longer antenna scapes prevailed in habitats with a dense herb / grass layer. Our study suggests that vegetation structural complexity can act as an environmental filter, driving ant assemblages in terms of both species numbers and functional traits. Our results can be used to predict turnover patterns in ant assemblages due to changes in management practices

The role of flies as pollinators of horticultural crops : an Australian case study with worldwide relevance

Australian horticulture relies heavily on the introduced managed honey bee, Apis mellifera Linnaeus 1758 (Hymenoptera: Apidae), to pollinate crops. Given the risks associated with reliance upon a single species, it would be prudent to identify other taxa that could be managed to provide crop pollination services. We reviewed the literature relating to the distribution, efficiency and management potential of a number of flies (Diptera) known to visit pollinator-dependent crops in Australia and worldwide. Applying this information, we identified the taxa most suitable to play a greater role as managed pollinators in Australian crops. Of the taxa reviewed, flower visitation by representatives from the dipteran families Calliphoridae, Rhiniidae and Syrphidae was frequently reported in the literature. While data available are limited, there was clear evidence of pollination by these flies in a range of crops. A review of fly morphology, foraging behaviour and physiology revealed considerable potential for their development as managed pollinators, either alone or to augment honey bee services. Considering existing pollination evidence, along with the distribution, morphology, behaviour and life history traits of introduced and endemic species, 11 calliphorid, two rhiniid and seven syrphid species were identified as candidates with high potential for use in Australian managed pollination services. Research directions for the comprehensive assessment of the pollination abilities of the identified taxa to facilitate their development as a pollination service are described. This triage approach to identifying species with high potential to become significant managed pollinators at local or regional levels is clearly widely applicable to other countries and taxa

Cryptic male dimorphism and fighting in a fig wasp

In some nonpollinating fig wasps, male competition for mates often results in serious injury or death. We studied the factors associated with fighting behaviour in an undescribed Philotrypesis fig wasp species. We quantified morphological traits in 440 males and revealed the presence of two discrete, but cryptic, male morphs, termed ‘aggressive’ (A) and ‘passive’ (P). For a given head size, morph A had larger mandibles. However, the body size distributions of the two morphs overlapped considerably, such that morph designation required calculation of the ratio of mandible (weapon) size to head size. Importantly, this means that standard analyses for dimorphism do not identify the two morphs correctly. We also sampled 62 pairs of males engaged in escalated fights and compared their size matching with that of randomly chosen pairs of males from the same patch. There was a significantly greater discrepancy in mandible size in fighting pairs than in randomly chosen pairs of males. Furthermore, our cryptic morph designation revealed the process underlying this pattern, as follows. Although only 22% of males were morph A, 45% of these males were involved in fights. In contrast, 78% of males were morph P, but only 16% of them were involved in fights. The different population frequencies and fighting tendencies of the two morphs combine to ensure that most fights occur between ‘heteromorphic’ pairs and this, in turn, generates the significant jaw size discrepancy recorded between fighting males

The dominant exploiters of the fig/pollinator mutualism vary across continents, but their costs fall consistently on the male reproductive function of figs

1. Fig trees (Moraceae: Ficus) are keystone species, whose ecosystem function relies on an obligate mutualism with wasps (Chalcidoidea: Agaonidae) that enter fig syconia to pollinate. Each female flower produces one seed (fig female reproductive function), unless it also receives a wasp egg, in which case it supports a wasp. Fig male reproductive function requires both male flowers and pollinator offspring, which are the only vectors of fig pollen. 2. The mutualism is exploited by other wasps that lay eggs but provide no pollination service. Most of these non-pollinating fig wasps (NPFWs) do not enter syconia, but lay eggs through the wall with long ovipositors. Some are gall-makers, while others are parasitoids or lethal inquilines of other wasps. 3. Ficus is pan-tropical and contains >750 fig species. However, NPFW communities vary across fig lineages and continents and their effects on the mutualism may also vary. This provides a series of natural experiments to investigate how the costs to a keystone mutualism vary geographically. 4. We made the first detailed study of the costs of NPFWs in a fig (Ficus obliqua G. Forst) from the endemic Australasian section Malvanthera. In contrast to the communities associated with section Americana in the New World, wasps from the subfamily Sycoryctinae (Chalcidoidea: Pteromalidae) dominated this community. 5. These sycoryctine wasps have a negative impact on pollinator offspring numbers, but not on seed production. Consequently, while the NPFW fauna varies greatly at high taxonomic levels across continents, we show that the consistent main effect of locally dominant exploiters of the mutualism is to reduce fig male reproductive function

Effects of within-tree flowering asynchrony on the dynamics of seed and wasp production in an Australian fig species

Within-tree flowering asynchrony in figs, which may allow pollinating wasps to avoid the risks of dispersal in inclement conditions, has been predicted as a trait to be favoured in highly seasonal environments. Comparisons of such asynchronous figs with better-known species that exhibit within-tree synchrony might also be expected to reveal differences in the outcome of the conflict between pollinator wasp and fig seed production, and the dynamics of non-pollinating wasps. This paper presents data on wasp and seed production in Ficus rubiginosa Desf. ex Vent., an asynchronous species that occurs in the highly seasonal environment of south-eastern Australia. In contrast to recent studies of figs showing within-tree flowering synchrony, syconium size was the main determinant of wasp and seed production in F. rubiginosa. Non-pollinating wasps were highly prevalent but occurred in low numbers and appeared to have relatively little impact on pollinator wasp or fig seed production. Data on flower positions revealed that non-pollinating wasps occurred almost exclusively in the outer layer of flowers, while pollinators were more abundant in the inner flower layer, which may represent an area of enemy-free space. The ratio of seeds to female pollinator wasps, an index of fig sex allocation, was more seed-biased than in several New World fig species that exhibit within-tree synchrony. This last result supports the idea that within-tree fruiting asynchrony permits a degree of self-pollination in F. rubiginosa

Spatial stratification of internally and externally non-pollinating gig wasps and their effects on pollinator and seed abundance in Ficus burkei

Fig trees (Ficus spp.) are pollinated by tiny wasps that enter their enclosed inflorescences (syconia). The wasp larvae also consume some fig ovules, which negatively affects seed production. Within syconia, pollinator larvae mature mostly in the inner ovules whereas seeds develop mostly in outer ovules—a stratification pattern that enables mutualism persistence. Pollinators may prefer inner ovules because they provide enemy-free space from externally ovipositing parasitic wasps. In some Australasian Ficus, this results in spatial segregation of pollinator and parasite offspring within syconia, with parasites occurring in shorter ovules than pollinators. Australian figs lack non-pollinating fig wasps (NPFW) that enter syconia to oviposit, but these occur in Africa and Asia, and may affect mutualist reproduction via parasitism or seed predation. We studied the African fig, F. burkei, and found a similar general spatial pattern of pollinators and NPFWs within syconia as in Australasian figs. However, larvae of the NPFW Philocaenus barbarus, which enters syconia, occurred in inner ovules. Philocaenus barbarus reduced pollinator abundance but not seed production, because its larvae replaced pollinators in their favoured inner ovules. Our data support a widespread role for NPFWs in contributing to factors preventing host overexploitation in fig-pollinator mutualisms