Floral constraint resulting from intersexual mimicry in a gynodioecious fig tree

Fig trees (Ficus: Moraceae) are pollinated by female fig wasps (Agaonidae) whose larvae develop inside galled flowers of unusual inflorescences (figs). Most fig trees also support communities of non‐pollinating fig wasps. Figs of different species display great size variation and contain tens to tens of thousands of flowers. Around one‐half the species of fig trees have the gynodioecious breeding system, where female trees have figs that produce seeds and male trees have figs that support development of pollinators. Mutual mimicry between receptive male and female figs ensures that pollinators enter female figs, even though the insects will die without reproducing, but the need to give no sex‐specific cues to the pollinators may constrain differences in size between receptive male and female figs. We compared relationships between inflorescence size and some measures of reproductive success in male and female figs of Ficus montana grown under controlled conditions in the presence of the pollinator Kradibia tentacularis and its main parasitoid Sycoscapter sp. indesc. Female figs that contained more flowers produced more seeds, but male figs did not increase the production of female pollinator K. tentacularis fig wasps in proportion of the flower number. Although more flowers were galled by the pollinators in male figs containing more female flowers, the high larval mortality caused by parasitism and nutritional limitation prevented the increase in the production of adult female offspring. Selection may favor the increase in flower numbers within figs in female plants of F. montana, but contrarily constrain this attribute in male plants.     

Development and characterization of microsatellite markers for two dioecious Ficus species

Microsatellite markers for Ficus montana and Ficus septica were developed using genomic libraries enriched for di‐, tri‐ and tetranucleotide repeats. The subsets of five and three best scorable primer pairs were characterized on 24 F. montana and 36 F. septica individuals, respectively. For F. montana, loci showed five to 14 alleles per locus and expected heterozygosities ranged between 0.23 and 0.87. For F. septica, loci showed three to five alleles per locus and expected heterozygosities ranged between 0.36 and 0.49. Four primer pairs (two from each subset) cross‐amplified in the other species, indicating transportability of the markers within the genus Ficus.     

Evidence for Bastesian mimicry in a butterfly-pollinated orchid

Observations in the Cape Province, South Africa, showed that Disa ferruginea (Orchidaceae) is dependent on a single butterfly species— Meneris tulbaghia (Nymphalidae: Satyrinae)—for pollination. The flowers of D. ferruginea contain no food reward and, instead, appear to secure pollinator visits by imitating flowers which are nectar sources for the butterfly. A red-flowered form of D. ferruginea appears to mimic the red nectar-producing flowers of Tritoniopsis triticea (Iridaceae) in the south-western Cape, while an orange-flowered form of D. ferruginea appears to mimic the orange nectar-producing flowers of Kniphofia uvaria (Asphodelaceae) in the Langeberg Mountains. Reflectance spectra of the orchid's flowers closely match those of its putative models. Analysis of foraging movements of the butterfly in a mixed stand of D. ferruginea and T. triticea indicated that it does not discriminate between the nectarless orchid and the nectar-producing model. Populations of D. ferruginea which are sympatric with T. triticea have relatively high levels of pollination and fruit production, compared with populations where the orchid grows alone. Although other studies have reported relatively low fecundity in deceptive orchids, pollination and fruiting success in D. ferruginea compares favourably with a nectar-producing congener, Disa uniflora , which is also pollinated solely by M. tulbaghia.     

Documenting the Effect of Foundress Number in a Dioecious Fig, Ficus fistulosa, in Malaysia

We studied foundress number and its effect on seed production in a dioecious fig Ficus fistulosa in Sarawak, Malaysia. The effects of flowering time and the two-way interaction of flowering time and tree location on foundress number were statistically significant. A multiple regression indicated seed production increased significantly with the number of foundresses. Our results indicate that phenology and local ecological factors generate a large variance in foundress number, which in turn affects the reproductive success of F. fistulosa.     

Phenotypic selection on flowering phenology and size in two dioecious plant species with different pollen vectors

Dioecious plants may be pollinated biotically by animals or abiotically via wind or water currents. It has been hypothesized that these two types of pollen vectors might impose contrasting selective pressures on plant flowering phenology. In the present study we describe the flowering phenology of two sympatric dioecious species with contrasting pollination modes: Mercurialis perennis (wind‐pollinated) and Tamus communis (insect‐pollinated). We estimated selection differentials and gradients for flowering time and flowering synchrony. As flowering time might depend on the accumulation of enough internal resources, we also estimated direct and indirect selection on plant size. Both species have male‐biased sexual ratios, and males are bigger and produce larger flower displays than females, but only in T. communis do males bloom earlier and for longer than females. Selection gradients suggest that selection tends to favor early‐flowering females of T. communis. There is no evidence of direct current selection on the flowering phenology of M. perennis. Intersexual differences in phenology fit with sex allocation and sexual selection theories. As we hypothesized, phenology of the animal‐pollinated species is under stronger selection than that of the wind‐pollinated species and we discuss the potential role of pollen vectors in shaping the flowering phenologies of the study species.     

Sexual dimorphism and fruit production in a dioecious understory tree,Ilex opaca Ait.

Summary This study suggested that sexual selection is potentially an important factor in the maintenance of dioecy in the American holly, Ilex opaca (Aquifoliaceae). Sexual dimorphisms in flower production and phenology were highly significant in this understory tree. On average, individual males produced 7.4 times as many flowers as did female trees. Staminate flowers lasted only a single day, whereas pistillate flowers lasted 3–4 days, during which they showed no significant decline in their ability to produce fruit after pollination. Individual male trees opened their flower buds asynchronously during the season, maximizing the number of days they were in flower. Individual females opened their buds more synchronously, maximizing their floral display at one point in time. Females produced fruits in numbers that were somewhat less than proportional to their flower production. Fruit development was initiated from only 38.9% and 69.5% of pistillate flowers in 1987 and 1988, respectively. By the time of ripening, an average female had lost 62.3%, 24.3%, and 11.1% of its initial fruit crop in 1986, 1987, and 1988, respectively. The proportion of fruit lost in 1986 was independent of the number of fruit that initially began development. In 1988, artifically supplementing pollen to a large number of flowers failed to increase either fruit or seed production relative to control branches with unsupplemented flowers. This suggested that resource levels were likely more important than pollen availability in limiting female reproductive success. These observations on I. opaca were consistent with the expectations for a population in which male reproductive success continues to benefit from continued pollinator service and female reproductive success does not.     

Balearic lizards use chemical cues from a complex deceptive mimicry to capture attracted pollinators

Deceptive flowers from several plant species emit odors that mimic oviposition cues and attract female insects seeking for a laying site. Helicodiceros muscivorus is a species that emits an odor mimicking the foul smell of rotting meat and thereby attracts blowflies that usually oviposit on carcasses but are deceived into pollinating the plant. Thus, H. muscivorus is a striking case of pollination by brood‐site deception. The Balearic lizard, Podarcis lilfordi, exhibits remarkable interactions with dead horse arum. Balearic lizards, which sometimes forage on carcasses, are attracted to blooming dead horse arum. We showed experimentally that P. lilfordi can detect chemical cues from carcasses on cotton swabs and exhibits elevated tongue‐flick rates to carcass chemical cues compared to control stimuli. Lizards also detected and located hidden carcasses using only airborne chemical cues. The responses of lizards to chemical cues from the spadix of blooming dead horse arum were qualitatively and quantitatively similar to those to carcass odors. Therefore, the decay‐like odor that attracts blowflies for the plant's benefit also attracts lizards. This attraction may initially have been somewhat favorable for lizards that eat blowflies, but slightly unfavorable for plants because the lizards ate some pollinators. We suggest that lizards attracted by odor may have learned later to use the plant for thermoregulation and then consume its fruits, making the association more positive for lizards and benefitted arum by seed dispersal.     

Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus

Flowers of many angiosperms attract fly pollinators through mimicry of animal carrion and faeces. This phenomenon of “sapromyiophily” is also evident in the sporophytes of some mosses and fruiting bodies of “stinkhorn” fungi, both of which use flies as agents of spore dispersal. We studied the scent chemistry of a stinkhorn fungus (Clathrus archeri) and seven fly-pollinated plant species with foetid odours to determine the degree to which these organisms mimic the scent of carrion and faeces (reference scent samples were collected from rotting meat, a rat carcass and horse and dog faeces), as well as the degree of convergent evolution between the fungus and angiosperm flowers. We found that scents of both the fungus and angiosperms tended to contain compounds typical of carrion, such as oligosulphides, and of faeces, such as phenol, indole and p-cresol. This study provides compelling new evidence for mimicry of carrion and faeces, as well as a striking pattern of convergence in the putrid scents of the fungus and the angiosperms, relative to those of confamilial species. The syndrome of sapromyiophily thus encompasses at least two kingdoms (Plantae and Fungi) and provides an effective means of exploiting flies as agents of pollen and spore dispersal.     

One fig to bind them all: host conservatism in a fig wasp community unraveled by cospeciation analyses among pollinating and nonpollinating fig wasps

The study of chalcid wasps that live within syconia of fig trees (Moraceae, Ficus ), provides a unique opportunity to investigate the evolution of specialized communities of insects. By conducting cospeciation analyses between figs of section Galoglychia and some of their associated fig wasps, we show that, although host switches and duplication have evidently played a role in the construction of the current associations, the global picture is one of significant cospeciation throughout the evolution of these communities. Contrary to common belief, nonpollinating wasps are at least as constrained as pollinators by their host association in their diversification in this section. By adapting a randomization test in a supertree context, we further confirm that wasp phylogenies are significantly congruent with each other, and build a "wasp community" supertree that retrieves Galoglychia taxonomic subdivisions. Altogether, these results probably reflect wasp host specialization but also, to some extent, they might indicate that niche saturation within the fig prevents recurrent intrahost speciation and host switching. Finally, a comparison of ITS2 sequence divergence of cospeciating pairs of wasps suggests that the diversification of some pollinating and nonpollinating wasps of Galoglychia figs has been synchronous but that pollinating wasps exhibit a higher rate of molecular evolution.     

Convergence of chemical mimicry in a guild of aphid predators

Abstract.  1. A variety of insects prey on honeydew-producing Homoptera and many do so even in the presence of ants that tend, and endeavour to protect, these trophobionts from natural enemies. Few studies have explored the semiochemical mechanisms by which these predators circumvent attack by otherwise aggressive ants.
2. Ants use specific mixtures of cuticular hydrocarbons (CHCs) as recognition labels, but this simple mechanism is frequently circumvented by nest parasites that engage in 'chemical mimicry' of their host ants by producing or acquiring a critical suite of these CHCs.
3. Analysis of the CHCs from the North American woolly alder aphid, Prociphilus tessellatus (Homoptera: Aphididae), their tending ants, and aphid predators from three insect orders, Feniseca tarquinius (Lepidoptera: Lycaenidae), Chrysopa slossonae (Neuroptera: Chrysopidae), and Syrphus ribesii (Diptera: Syrphidae), showed that while the CHC profile of each predatory species was distinct, each was chemically more similar to the aphids than to either tending ant species. Further, the CHCs of each predator species were a subset of the compounds found in the aphids' profile.
4. These results implicate CHCs as a recognition cue used by ants to discriminate trophobionts from potential prey and a probable mechanism by which trophobiont predators circumvent detection by aphids and their tending ants.
5. Although several features of the aphids' CHC profile are shared among the chemically mimetic taxa, variation in the precision of mimicry among the members of this predatory guild demonstrates that a chemical mimic need not replicate every feature of its model.     

Evidence for the circadian gene period as a proximate mechanism of protandry in a pollinating fig wasp

Protandry in insects is the tendency for adult males to emerge before females and usually results from intra-sexual selection. However, the genetic basis of this common phenomenon is poorly understood. Pollinating fig wasp (Agaonidae) larvae develop in galled flowers within the enclosed inflorescences (‘figs’) of fig trees. Upon emergence, males locate and mate with the still galled females. After mating, males release females from their galls to enable dispersal. Females cannot exit galls or disperse from a fig without male assistance. We sampled male and female Ceratosolen solmsi (the pollinator of Ficus hispida) every 3 h over a 24 h emergence period, and then measured the expression of five circadian genes: period (per), clock (clk), cycle (cyc), pigment-dispersing factor (pdf) and clockwork orange (cwo). We found significant male-biased sexual dimorphism in the expression of all five genes. per showed the greatest divergence between the sexes and was the only gene rhythmically expressed. Expression of per correlated closely with emergence rates at specific time intervals in both male and female wasps. We suggest that this rhythmical expression of per may be a proximate mechanism of protandry in this species.     

Sexual and vegetative reproduction in the aboveground part of a dioecious clonal plant, <Emphasis Type="Italic">Dioscorea japonica</Emphasis> (Dioscoreaceae)

In dioecious clonal plants, the reproductive effort required to set seeds will be responsible for the larger investment in sexual reproduction by females. If there will be a trade-off in resource allocation between sexual and clonal reproduction, this differential sexual reproduction will lead to sexual differentiation in the relative amount of clonal reproduction. To test this prediction, we studied differences between the sexes in their phenologies and investments in sexual and vegetative reproduction (clonal reproduction by means of bulbils) with respect to ramet size in a dioecious clonal plant, Dioscorea japonica Thunb. The period of bulbil production overlapped the period during which infructescences developed. Females flowered later, produced heavier inflorescences, and fewer flowers per inflorescence than did males. Regression analysis using the size of the individual plants demonstrated that large females made smaller investments in inflorescences and larger investments in sexual reproduction than did large males. In contrast, females invested fewer resources in vegetative reproduction than did males. However, the total investments in sexual and vegetative reproduction did not differ between the sexes. These results supported our hypothesis on the sexual differentiation in sexual and clonal reproduction.     

No association between mitochondrial DNA haplotypes and a female-limited mimicry phenotype in Papilio glaucus

Abstract Alternative alleles at a locus on the W chromosome of Papilio glaucus (causing dark or yellow wing colors, respectively) underlie a female-limited mimicry polymorphism thought to be maintained by balancing selection. In species with heterogametic females (i.e., the ZZ-male/ZW-female sex chromosome system), the mitochondrial DNA and the W chromosome are genetically linked because they are both maternally transmitted. We investigate the association of COI and COII mitochondrial DNA haplotypes with alternative W-linked phenotypes. Surprisingly, we find no congruence between mitochondrial DNA genealogies and inferred W-linked color alleles in P. glaucus. Using a maximum-likelihood phylogenetic approach, we reject the hypothesis of monophyly for darkmorph mitochondrial DNA lineages, even in the presence of putative low-frequency mimicry suppressor alleles or alternative melanizing factors. The most likely genealogical tree topologies assume more than one exchange event between mitochondrial DNA cytotype and the W-linked color morph. These results suggest that there is either paternal leakage of mitochondrial DNA or that more than two W-linked alleles underlie the alternative color morphs. Using data from an additional mitochondrial DNA locus, ND5, we show that pairwise linkage disequilibrium decays with physical distance between polymorphic sites. This finding suggests that genetic exchanges between maternal and paternal mitochondrial DNAs may have contributed to the lack of association we observe between phenotype and genotype.     

Facultative mimicry: cues for colour change and colour accuracy in a coral reef fish

Mimetic species evolve colours and body patterns to closely resemble poisonous species and thus avoid predation (Batesian mimicry), or resemble beneficial or harmless species in order to approach and attack prey (aggressive mimicry). Facultative mimicry, the ability to switch between mimic and non-mimic colours at will, is uncommon in the animal kingdom, but has been shown in a cephalopod, and recently in a marine fish, the bluestriped fangblenny Plagiotremus rhinorhynchos, an aggressive mimic of the juvenile cleaner fish Labroides dimidiatus. Here we demonstrate for the first time that fangblennies adopted mimic colours in the presence of juvenile cleaner fish; however, this only occurred in smaller individuals. Field data indicated that when juvenile cleaner fish were abundant, the proportion of mimic to non-mimic fangblennies was greater, suggesting that fangblennies adopt their mimic disguise depending on the availability of cleaner fish. Finally, measurements of spectral reflectance suggest that not only do mimic fangblennies accurately resemble the colour of their cleaner fish models but also mimic other species of fish that they associate with. This study provides insights into the cues that control this remarkable facultative mimicry system and qualitatively measures its accuracy.     

Evidence for aggressive mimicry in an adult brood parasitic bird,and generalized defences in its host

Mimicry of a harmless model (aggressive mimicry) is used by egg, chick and fledgling brood parasites that resemble the host''s own eggs, chicks and fledglings. However, aggressive mimicry may also evolve in adult brood parasites, to avoid attack from hosts and/or manipulate their perception of parasitism risk. We tested the hypothesis that female cuckoo finches (Anomalospiza imberbis) are aggressive mimics of female Euplectes weavers, such as the harmless, abundant and sympatric southern red bishop (Euplectes orix). We show that female cuckoo finch plumage colour and pattern more closely resembled those of Euplectes weavers (putative models) than Vidua finches (closest relatives); that their tawny-flanked prinia (Prinia subflava) hosts were equally aggressive towards female cuckoo finches and southern red bishops, and more aggressive to both than to their male counterparts; and that prinias were equally likely to reject an egg after seeing a female cuckoo finch or bishop, and more likely to do so than after seeing a male bishop near their nest. This is, to our knowledge, the first quantitative evidence for aggressive mimicry in an adult bird, and suggests that host–parasite coevolution can select for aggressive mimicry by avian brood parasites, and counter-defences by hosts, at all stages of the reproductive cycle.     

Longevity, early emergence and body size in a pollinating fig wasp--implications for stability in a fig-pollinator mutualism

1. Fig trees (Ficus) are pollinated only by agaonid wasps, whose larvae also gall fig ovules. Each ovule develops into either a seed (when pollinated) or a wasp (when an egg is also laid inside) but not both. 2. Ovipositing wasps (foundresses) favour ovules near the centre of the enclosed inflorescence (syconium or 'fig'), leaving ovules near the outer wall to develop into seeds. This spatial stratification of wasps and seeds ensures reproduction in both partners, and thereby enables mutualism persistence. However, the mechanism(s) responsible remain(s) unknown. 3. Theory shows that foundresses will search for increasingly rare inner ovules and ignore outer ovules, as long as ovipositing in outer ovules is sufficiently slow and/or if inner ovules confer greater fitness to wasps. The fig-pollinator mutualism can therefore be stabilized by strong time constraints on foundresses and by offspring fitness gradients over variation in ovule position. 4. Female fig wasps cannot leave their galls without male assistance. We found that females in outer ovules were unlikely to be released. Inner ovules thus have added value to foundresses, because their female offspring are more likely to mate and disperse. 5. For those offspring that did emerge, gall position (inner/outer) and body size did not influence the order in which female pollinators exited syconia, nor did early emerging wasps enjoy increased life spans. 6. We also found that the life spans of female wasps nearly doubled when given access to moisture. We suggest that conflict resolution in the fig-pollinator mutualism may thus be influenced by tropical seasonality, because wasps may be less able to over-exploit ovules in dry periods due to time constraints.     

Genetic differences among populations in sexual dimorphism: evidence for selection on males in a dioecious plant

Genetic variation among populations in the degree of sexual dimorphism may be a consequence of selection on one or both sexes. We analysed genetic parameters from crosses involving three populations of the dioecious plant Silene latifolia, which exhibits sexual dimorphism in flower size, to determine whether population differentiation was a result of selection on one or both sexes. We took the novel approach of comparing the ratio of population differentiation of a quantitative trait (Q(ST) ) to that of neutral genetic markers (F(ST) ) for males vs. females. We attributed 72.6% of calyx width variation in males to differences among populations vs. only 6.9% in females. The Q(ST) /F(ST) ratio was 4.2 for males vs. 0.4 for females, suggesting that selection on males is responsible for differentiation among populations in calyx width and its degree of sexual dimorphism. This selection may be indirect via genetic correlations with other morphological and physiological traits.     

Evidence of a direct chemical plant defense role for maltol against spruce budworm

This study examines the direct chemical defensive role of maltol, a previously identified secondary metabolite found in balsam fir, Abies balsamea (L.) Mill. (Pinaceae), that was detected during herbivory of spruce budworm, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae). Although used extensively in many industries, in addition to being found in multiple plant species, its functional role in plants remains unknown. The objectives of this study were to quantify the amount of free maltol and its potential conjugated form, maltol glucoside, in various foliage age classes and to evaluate whether constitutive foliage levels of maltol have an impact on spruce budworm fitness in maltol supplementation assays. Gas chromatography–mass spectrometry (GC‐MS) analysis of balsam fir foliage showed that maltol is produced in all foliage age classes tested; however, concentrations were significantly higher in older foliage. Liquid chromatography–mass spectrometry–mass spectrometry (LC‐MS‐MS) analysis showed that maltol also exists in balsam fir in its glucosylated form, a unique discovery in conifers. Similar to maltol, maltol glucoside is also present in current and 1‐year‐old balsam fir foliage and in significantly higher concentration in older foliage. We investigated the impact of maltol‐treated diet on spruce budworm fitness. Maltol additions that reflected constitutive foliage concentrations caused a significant reduction in larval development rate and pupal mass, whereas higher concentrations were required to cause significant mortality. These results suggest that maltol may be an important component of a direct defense strategy in balsam fir against spruce budworm herbivory.     

Independent evolution of sexual dimorphism and female‐limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)

Several species of swallowtail butterflies (genus Papilio) are Batesian mimics that express multiple mimetic female forms, while the males are monomorphic and nonmimetic. The evolution of such sex‐limited mimicry may involve sexual dimorphism arising first and mimicry subsequently. Such a stepwise scenario through a nonmimetic, sexually dimorphic stage has been proposed for two closely related sexually dimorphic species: Papilio phorcas, a nonmimetic species with two female forms, and Papilio dardanus, a female‐limited polymorphic mimetic species. Their close relationship indicates that female‐limited polymorphism could be a shared derived character of the two species. Here, we present a phylogenomic analysis of the dardanus group using 3964 nuclear loci and whole mitochondrial genomes, showing that they are not sister species and thus that the sexually dimorphic state has arisen independently in the two species. Nonhomology of the female polymorphism in both species is supported by population genetic analysis of engrailed, the presumed mimicry switch locus in P. dardanus. McDonald–Kreitman tests performed on SNPs in engrailed showed the signature of balancing selection in a polymorphic population of P. dardanus, but not in monomorphic populations, nor in the nonmimetic P. phorcas. Hence, the wing polymorphism does not balance polymorphisms in engrailed in P. phorcas. Equally, unlike in P. dardanus, none of the SNPs in P. phorcas engrailed were associated with either female morph. We conclude that sexual dimorphism due to female polymorphism evolved independently in both species from monomorphic, nonmimetic states. While sexual selection may drive male–female dimorphism in nonmimetic species, in mimetic Papilios, natural selection for protection from predators in females is an alternative route to sexual dimorphism.     

Causes of secondary sexual differences in plants — Evidence from extreme leaf dimorphism in Leucadendron (Proteaceae)

In extreme cases leaves in male plants of the dioecious genus Leucadendron (Proteaceae) are up to an order of magnitude smaller than female leaves. This secondary sexual dimorphism (SSD) in leaf size has previously been suggested to be due to intra-male sexual selection, leading to an increase in male allocation to reproduction in dimorphic species. After critically evaluating previous data provided to support this hypothesis, I suggest on both theoretical grounds and on re-analysis that this argument is unlikely and unsupported. Leaf size dimorphism could theoretically evolve directly due to disruptive ecological selection between genders, leading to niche dimorphism either within or between habitats. I test this ecological causation hypothesis by providing data on specific leaf area (sla) and water use efficiency (δ ¹³C) of leaves from males and females of several Leucadendron species. Results confirm the expectation of minimal gender differences. I argue that leaf dimorphism is a consequence of selection on flower size and architecture.