Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been influential study systems for coevolutionary biology. These mutualisms include those between figs and fig wasps, yuccas and yucca moths, leafflowers and leafflower moths, globeflowers and globeflower flies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species‐specificity of some of these mutualisms have been cited as evidence that coevolution between plants and pollinators drives their mutual diversification. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We find that most species‐rich brood pollination mutualisms show significant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict‐sense contemporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host‐shifts appear to be common, and widespread host‐shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a “coevolution through cospeciation” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity.     

小果叶下珠花气味组成及其两性异型性

大戟科(Euphorbiaceae)植物小果叶下珠(Phyllanthus microcarpus)由种特异性细蛾科(Gracillariidae)昆虫头细蛾(Epicephala)专门为其传粉,具体包括:头细蛾在雄花上积极采粉,然后为雌花授粉并在其内产卵等极其不同的传粉行为。花气味在维持小果叶下珠与传粉头细蛾专性传粉互利共生关系中起着至关重要的作用。采用动态顶空吸附法分别收集小果叶下珠雌花和雄花气味,利用气相色谱-质谱(gas chromatography-mass spectrometry,GC-MS)联用技术分析鉴定其成分,并用峰面积归一法与内标法进行定量,最后通过主成分分析法比较两者间的差异性。结果表明:(1)小果叶下珠花气味中共分离出17种化合物,主要以萜类和脂肪族物质为主;顺-β-罗勒烯在雌花和雄花中含量均最高,为主要气味成分;(2)雌花气味释放量显著高于雄花;(3)雌花和雄花之间气味化学成分存在明显的差异,即具有两性异形性。初步推测花气味出现两性异形性是植物为适应传粉头细蛾极其高度特异的传粉行为(雄花采粉,雌花传粉并产卵)而选择进化的结果。     

Does acoustic priming ‘sweeten the pot’ of floral nectar?

A recent claim that evening primrose flowers adaptively secrete nectar in response to vibrations from hovering bees lacks supporting evidence. The authors fail to demonstrate that bees can access the concealed nectar and that their visits enhance plant fitness. Reanalysis of the authors’ data raises additional concerns about their conclusions.     

The evolutionary ecology of cheating: does superficial oviposition facilitate the evolution of a cheater yucca moth?

Abstract 1. A major question in the study of mutualism is to understand how mutualists may revert to antagonists that exploit the mutualism (i.e. switch to cheating). In the classic pollination mutualism between yuccas and yucca moths, the cheater moth Tegeticula intermedia is sister to the pollinator moth T. cassandra. These moth species have similar ovipositor morphology, but T. intermedia emerges later, oviposits into fruit rather than flowers, and does not pollinate. 2. We tested if the pollinator, T. cassandra, was pre‐adapted to evolve a cheater lineage by comparing its emergence and oviposition behaviour on yucca fruit to a distantly related pollinator, T. yuccasella, that differs in ovipositor morphology and oviposition behaviour. We predicted that if T. cassandra was pre‐adapted to cheat, then these pollinators would emerge later and be able to oviposit into fruit in contrast to T. yuccasella. 3. Contrary to expectations, a common garden‐rearing experiment demonstrated that emergence of T. cassandra was not significantly delayed relative to T. yuccasella. Moth emergence patterns overlapped broadly. 4. No choice oviposition experiments with female moths demonstrated that both pollinator species attempted to oviposit into fruit, but only T. cassandra was successful. Four out of 84 T. cassandra successfully oviposited into older fruit, whereas zero out of 79 T. yuccasella oviposited into older fruit. The rarity of the cheating behaviour in pollinators, however, meant that no significant difference in oviposition ability was detected. 5. The results suggest that a shift in emergence phenology is likely not a pre‐adaptation to the evolution of cheating, but that the ability to successfully lay eggs into fruit may be. The results also demonstrate that cheating attempts are rare in these pollinator species and, hence, the evolutionary transition rate from pollinator to cheater is likely to be low.     

Assessment of the diversity and species specificity of the mutualistic association between Epicephala moths and Glochidion trees

The obligate mutualisms between flowering plants and their seed-parasitic pollinators constitute fascinating examples of interspecific mutualisms, which are often characterized by high levels of species diversity and reciprocal species specificity. The diversification in these mutualisms has been thought to occur through simultaneous speciation of the partners, mediated by tight reciprocal adaptation; however, recent studies cast doubt over this general view. In this study, we examine the diversity and species specificity of Epicephala moths (Gracillariidae) that pollinate Glochidion trees (Phyllanthaceae), using analysis of mitochondrial and nuclear gene sequences. Phylogenetic analysis of Epicephala moths associated with five Glochidion species in Japan and Taiwan reveal six genetically isolated species that are also distinguishable by male genital morphology: (i) two species specific to single host species (G. acuminatum and G. zeylanicum, respectively); (ii) two species that coexist on G. lanceolatum; and (iii) two species that share two, closely-related parapatric hosts (G. obovatum and G. rubrum). Statistical analysis shows that the two species associated with G. lanceolatum are not sister species, indicating the colonization of novel Glochidion host in at least one lineage. Behavioural observations suggest that all six species possess the actively-pollinating habit, thus none of the studied species has become a nonmutualistic 'cheater' that exploits the benefit resulting from pollination by other species. Our results parallel recent findings in ecologically similar associations, namely the fig-fig wasp and yucca-yucca moth mutualisms, and contribute to a more general understanding of the factors that determine ecological and evolutionary outcomes in these mutualisms.     

Infertile seeds ofYucca schottii: A beneficial role for the plant in the yucca-yucca moth mutualism?

Summary The yucca-yucca moth interaction is a classic case of obligate mutualism. Female moths pollinate and oviposit in the gynoecium of the flower; however, maturing larvae eat a fraction of the developing seeds. We studied within-fruit distributions of four seed types (fertile, infertile, eaten and uneaten seeds) in order to evaluate costs and benefits in aYucca schottii population in southeastern Arizona. We focused on how the spatial arrangement of seeds affected larval behaviour and, hence, the costs of the mutualism to the yucca. Infertile seeds were distributed throughout both infested and uninfested locules. Additionally, moth larvae feeding in a single locule preferred fertile seeds and even avoided infertile seeds and left the fruit significantly more often when they encountered infertile seeds. We suggest that, regardless of the cause of infertile seeds, they function as blocking units within seed locules and therefore reduce seed predation by moth larvae. We also suggest that, together with certain other fruit traits, the presence of infertile seeds promotes the evolutionary stability of this pollination mutualism.     

宽瓣头细蛾形态及生物学特性研究

宽瓣头细蛾Epicephala lativalvaris Li, Wang & Zhang是最近发现在黑面神Breynia fruticosa和喙果黑面神B. rostrata上专性传粉的昆虫。通过野外观察宽瓣头细蛾的访花行为、 室内饲养宽瓣头细蛾幼虫及解剖黑面神和喙果黑面神果实, 首次对其个体发育过程中各虫态的形态特征及生活习性和生活史进行了详细研究。结果表明： 宽瓣头细蛾的生活史因气候的不同而出现差异, 其在福建厦门1年发生4~5代, 有4个羽化主要高峰期, 分别为5月上旬至中旬、 6月中旬至下旬、 8月及9月下旬至10月上旬, 11月中下旬有少数成虫羽化, 12月上旬至次年4月中旬以卵或蛹越冬; 而在海南鹦哥岭1年发生6代, 无越冬现象。成虫分别主动为黑面神或喙果黑面神传粉并将卵产于子房内, 幼虫以寄主植物种子为食, 需要消耗果实内全部6粒种子才能发育成熟, 但每个种群内留有20.37%~77.63%完好的果实, 以维持互利关系的稳定。两种植物的结实率近似, 但宽瓣头细蛾对喙果黑面神的果实危害率是黑面神的2.05倍。结果说明, 在宽瓣头细蛾 黑面神和喙果黑面神专性传粉互利共生关系中, 两种寄主植物所获得的利益近似, 但喙果黑面神为宽瓣头细蛾提供了更多的回报。研究结果为头细蛾属其他种类生物学特性的了解提供了借鉴, 并为探讨宽瓣头细蛾 黑面神和喙果黑面神专性传粉互利共生关系稳定性的维持机制提供了基本依据。     

Floral morphology and pollination in Gastrodia elata,a mycoheterotrophic orchid

Pollination biology in Gastrodia elata was investigated on Rebun Island, Japan. The flowers have an urceolate perianth chamber whose opening is constricted by the column and labellum. This structure plays a crucial role in the selection of small‐bodied bees from flower visitors of various body sizes. In addition, the furrow on the ventral side of the column possibly contributes to the admission of sweat bee pollinators, whose thoracic widths match the width of the furrow. Sweat bees receive the pollinarium on their thorax while escaping head first from the chamber. No pollinator rewards, such as previously reported harvestable spongy tissue, are likely to be produced by the orchid. The flowers, however, have a glossy area reminiscent of nectar secreted into the chamber that likely acts as a deceptive signal for pollinators. Fruit‐set ratios were found to vary spatiotemporally; the values were higher under bright light conditions, probably reflecting the presence of sweat bees for sunny places.     

Are Drosophila preferences for yeasts stable or contextual?

Whether there are general mechanisms, driving interspecific chemical communication is uncertain. Saccharomycetaceae yeast and Drosophila fruit flies, both extensively studied research models, share the same fruit habitat, and it has been suggested their interaction comprises a facultative mutualism that is instigated and maintained by yeast volatiles. Using choice tests, experimental evolution, and volatile analyses, we investigate the maintenance of this relationship and reveal little consistency between behavioral responses of two isolates of sympatric Drosophila species. While D. melanogaster was attracted to a range of different Saccharomycetaceae yeasts and this was independent of fruit type, D. simulans preference appeared specific to a particular S. cerevisiae genotype isolated from a vineyard fly population. This response, however, was not consistent across fruit types and is therefore context‐dependent. In addition, D. simulans attraction to an individual S. cerevisiae isolate was pliable over ecological timescales. Volatile candidates were analyzed to identify a common signal for yeast attraction, and while D. melanogaster generally responded to fermentation profiles, D. simulans preference was more discerning and likely threshold‐dependent. Overall, there is no strong evidence to support the idea of bespoke interactions with specific yeasts for either of these Drosophila genotypes. Rather the data support the idea Drosophila are generally adapted to sense and locate fruits infested by a range of fungal microbes and/or that yeast–Drosophila interactions may evolve rapidly.