Fig Wasps: Mechanism of Pollen Transfer

Ramírez, B William

doi:10.1126/science.163.3867.580

Cited by 77 publications

(13 citation statements)

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“…These features aid in pollen collection and prevent access by less effective pollinators to pollen and nectar resources. Pollinators too, have evolved specialized morphological adaptations such as combs, pockets [15] and tentacles [16] with which to capture and manipulate pollen. In addition, many pollinators use these traits to deposit pollen deliberately through stereotyped behaviors, known as active pollination [17].…”

Section: Introductionmentioning

confidence: 99%

Two’s company, three’s a crowd: co-occurring pollinators and parasite species in Breynia oblongifolia (Phyllanthaceae)

et al. 2018

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BackgroundObligate pollination mutualisms (OPMs) are specialized interactions in which female pollinators transport pollen between the male and female flowers of a single plant species and then lay eggs into those same flowers. The pollinator offspring hatch and feed upon some or all of the developing ovules pollinated by their mothers. Strong trait matching between plants and their pollinators in OPMs is expected to result in reciprocal partner specificity i.e., a single pollinator species using a single plant species and vice versa, and strict co-speciation. These issues have been studied extensively in figs and fig wasps, but little in the more recently discovered co-diversification of Epicephala moths and their Phyllanthaceae hosts. OPMs involving Epicephala moths are believed occur in approximately 500 species of Phyllanthaceae, making it the second largest OPM group after the Ficus radiation (> 750 species). In this study, we used a mixture of DNA barcoding, genital morphology and behavioral observations to determine the number of Epicephala moth species inhabiting the fruits of Breynia oblongifolia, their geographic distribution, pollinating behavior and phylogenetic relationships.ResultsWe found that B. oblongifolia hosts two species of pollinator that co-occurred at all study sites, violating the assumption of reciprocal specificity. Male and female genital morphologies both differed considerably between the two moth species. In particular, females differed in the shape of their ovipositors, eggs and oviposition sites. Phylogenetic analyses indicated that the two Epicephala spp. on B. oblongifolia likely co-exist due to a host switch. In addition, we discovered that Breynia fruits are also often inhabited by a third moth, an undescribed species of Herpystis, which is a non-pollinating seed parasite.ConclusionsOur study reveals new complexity in interactions between Phyllantheae and Epicephala pollinators and highlights that host switching, co-speciation and non-pollinating seed parasites can shape species interactions in OPMs. Our finding that co-occurring Epicephala species have contrasting oviposition modes parallels other studies and suggests that such traits are important in Epicephala species coexistence.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1314-y) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Two’s company, three’s a crowd: co-occurring pollinators and parasite species in Breynia oblongifolia (Phyllanthaceae)

et al. 2018

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“…In these species females of pollinating wasps actively collect pollen from anthers before leaving their natal figs and place it in special thoracic structures called pollen pockets, in order to transport it to another fig whose pistillate flowers are receptive to pollination. Once inside a receptive fig, the female wasp removes some pollen from its pollen pockets each time it lays an egg and deposits it on the stigma surface (Galil and Eisikowitch, 1969;Ramírez -Benavides, 1969). In actively pollinated Ficus species, stigmata can be cohesive, forming a common surface for pollen tube germination (= synstigma).…”

Section: Introductionmentioning

confidence: 99%

Morphological diversity and function of the stigma in Ficus species (Moraceae)

et al. 2018

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The stigma plays several roles such as pollen hydration and selection, and pollen tube nutrition. In the Ficus-fig wasp mutualism, stigmata have an additional, almost unknown, function by representing a physical interface for both plant and wasp reproduction. We used light and electron microscopy to compare the detailed morphology of the stigmata of nine Ficus species of different sections and with different pollination modes and sexual expressions. Figs were collected at the stage when the stigmata were receptive for pollination. Stigmata in actively pollinated monoecious species have well developed papillae concentrated on the adaxial surface exposed towards the fig cavity. Conversely, the passively pollinated monoecious species have the whole surface of the stigmata covered by somewhat smaller papillae. In both actively and passively pollinated monoecious species these features are consistent, irrespective of style length. In all actively pollinated gynodioecious species, the stigmata of pistillate flowers were tubular or infundibuliform whereas in almost all actively pollinated monoecious species (except F. racemosa) the stigmata were filiform, with one branch or two asymmetric branches. In gynodioecious species the short-styled flowers in "male" figs show a limited receptive surface with small papillae, while the stigmata of long-styled flowers in "female" figs are covered by papillae that extend down the sides of the style, increasing the stigmatic surface. In actively pollinated species, stigmata are cohesive, forming a common surface for pollen tube germination (= synstigma). The synstigma arrangement was quite variable: lax, cohesive or very cohesive, with entanglement by stigmatic papillae and stylar trichomes. Entanglement by stylar trichomes is common in gynodioecious species. The synstigma arrangement did not correlate with phylogeny or breeding system. This study is the first to report a very loose synstigma in actively pollinated monoecious Ficus species. Our analyses revealed that, in Ficus, the synstigma is functionally analogous to an extra-gynoecial compitum. Comparative studies will be required to test further hypotheses about the evolutionary determinants of such variation.

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“…Based on the systematic survey of Kjellberg et al [19], almost two thirds of fig species are actively pollinated and the others are passively pollinated. Less pollen is produced in actively pollinated figs, in which fig wasps actively collect pollen from anthers, store them in special pollen pockets and deposit pollen efficiently on the stigmas within other receptive syconia using their forelegs [20]. In other fig wasps, the above behavior is absent and there are often neither coxal combs nor pollen pockets on their body.…”

Section: Introductionmentioning

confidence: 99%

Has Pollination Mode Shaped the Evolution of Ficus Pollen?

Wang

Chen

et al. 2014

PLoS ONE

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BackgroundThe extent to which co-evolutionary processes shape morphological traits is one of the most fascinating topics in evolutionary biology. Both passive and active pollination modes coexist in the fig tree (Ficus, Moraceae) and fig wasp (Agaonidae, Hymenoptera) mutualism. This classic obligate relationship that is about 75 million years old provides an ideal system to consider the role of pollination mode shifts on pollen evolution.Methods and Main FindingsTwenty-five fig species, which cover all six Ficus subgenera, and are native to the Xishuangbanna region of southwest China, were used to investigate pollen morphology with scanning electron microscope (SEM). Pollination mode was identified by the Anther/Ovule ratio in each species. Phylogenetic free regression and a correlated evolution test between binary traits were conducted based on a strong phylogenetic tree. Seventeen of the 25 fig species were actively pollinated and eight species were passively pollinated. Three pollen shape types and three kinds of exine ornamentation were recognized among these species. Pollen grains with ellipsoid shape and rugulate ornamentation were dominant. Ellipsoid pollen occurred in all 17 species of actively pollinated figs, while for the passively pollinated species, two obtuse end shapes were identified: cylinder and sphere shapes were identified in six of the eight species. All passively pollinated figs presented rugulate ornamentation, while for actively pollinated species, the smoother types - psilate and granulate-rugulate ornamentations - accounted for just five and two among the 17 species, respectively. The relationship between pollen shape and pollination mode was shown by both the phylogenetic free regression and the correlated evolution tests.ConclusionsThree pollen shape and ornamentation types were found in Ficus, which show characteristics related to passive or active pollination mode. Thus, the pollen shape is very likely shaped by pollination mode in this unique obligate mutualism.

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Fig Wasps: Mechanism of Pollen Transfer

Cited by 77 publications

References 3 publications

Two’s company, three’s a crowd: co-occurring pollinators and parasite species in Breynia oblongifolia (Phyllanthaceae)

Two’s company, three’s a crowd: co-occurring pollinators and parasite species in Breynia oblongifolia (Phyllanthaceae)

Morphological diversity and function of the stigma in Ficus species (Moraceae)

Has Pollination Mode Shaped the Evolution of Ficus Pollen?

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