Association between competition and obligate mutualism in a chemostat

In this paper, we consider a simple chemostat model involving two obligate mutualistic species feeding on a limiting substrate. Systems of differential equations are proposed as models of this association. A detailed qualitative analysis is carried out. We show the existence of a domain of coexistence, which is a set of initial conditions in which both species survive. We demonstrate, under certain supplementary assumptions, the uniqueness of the stable equilibrium point which corresponds to the coexistence of the two species.     

A novel obligate cultivation mutualism between damselfish and Polysiphonia algae

In cultivation mutualisms, farming animals prepare fields for cultivars, enhance their growth and harvest them. For example, in terrestrial ecosystems, plant-herbivore cultivation mutualisms arose between humans and their crops only relatively recently. We discovered an obligate cultivation mutualism between a damselfish and an alga in a coral reef ecosystem. The damselfish, Stegastes nigricans, manages algal farms through territorial defence against the invading grazers and through weeding of unpalatable algae. As a result, the algal farms of S. nigricans are dominated by one species, Polysiphonia sp. We performed an exhaustive survey of algal assemblages inside and outside the territories of five damselfish species around the Ryukyu Islands, Japan, using molecular and morphological characteristics. Polysiphonia sp. 1 grew exclusively inside the farms of S. nigricans, and never elsewhere. Since only Polysiphonia sp. 1 is harvested and consumed by the damselfish as a staple food, this interdependent relationship is an obligate cultivation mutualism. This is the first record of an obligate plant-herbivore cultivation mutualism in a marine ecosystem. Our data also suggest that three other Polysiphonia species are facultatively mutual with, commensal with, or parasitic on other damselfish species.     

传粉细蛾与大戟科植物专性授粉的互惠共生体系

在已知的昆虫与植物所形成的专性授粉互惠共生体系中,榕树—榕小蜂、丝兰—丝兰蛾体系是经典实例,国内外学者已经从不同角度进行了大量的研究,为我们理解植物—传粉者互惠共生体系协同进化的机理和历史积累了宝贵的资料。近些年的研究发现鳞翅目细蛾科头细蛾属昆虫与大戟科植物之间也存在相似的协同进化关系。文章对国内外学者有关传粉细蛾与大戟科植物互惠共生协同进化的研究进行了整理。     

Absence of population-level phenotype matching in an obligate pollination mutualism

Coevolution is thought to promote evolutionary change between demes that ultimately results in speciation. If this is the case, then we should expect to see similar patterns of trait matching and phenotypic divergence between populations and between species in model systems for coevolution. As measures of divergence are frequently only available at one scale (population level or taxon level), this contention is rarely tested directly. Here, we use the case of co-divergence between different varieties of Joshua tree Yucca brevifolia (Agavaceae) and their obligate pollinators, two yucca moths (Tegeticula spp. Prodoxidae), to test for trait matching between taxa and among populations. Using model selection, we show that there is trait matching between mutualists at the taxon level, but once we account for differences between taxa, there is no indication of trait matching in local populations. This result differs from similar studies in other coevolving systems. We hypothesize that this discrepancy arises because coevolution in obligate mutualisms favours divergence less strongly than coevolution in other systems, such as host–parasite interactions.     

Species coexistence under resource competition with intraspecific and interspecific direct competition in a chemostat

Competition theory has developed separately for direct competition and for exploitative competition. However, the combined effects of the two types of competition on species coexistence remain unclear. To examine how intraspecific and interspecific direct competition contributes to the coexistence of species competing for a single resource, we constructed a chemostat-type resource competition model. With general functions for intraspecific and interspecific direct competition, we derived necessary and sufficient conditions (except for a critical case that rarely occurs in a biological sense) that determine the number of stably coexisting species. From these conditions, we found that the number of coexisting species is determined just by the invasibility of each species into subcommunities with a smaller number of species. In addition, using a combination of rigorous mathematical theory and a simple graphical method, we can demonstrate how the stronger intraspecific direct competition facilitates species invasion, leading to a larger number of coexisting species.     

The cost of sex and competition between cyclical and obligate parthenogenetic rotifers

The ubiquity of sexual reproduction is an evolutionary puzzle because asexuality should have major reproductive advantages. Theoretically, transitions to asexuality should confer substantial benefits in population growth and lead to rapid displacement of all sexual ancestors. So far, there have been few rigorous tests of one of the most basic assumptions of the paradox of sex: that asexuals are competitively superior to sexuals immediately after their origin. Here I examine the fitness consequences of very recent transitions to obligate parthenogenesis in the cyclical parthenogenetic rotifer Brachionus calyciflorus. This experimental system differs from previous animal models, since obligate parthenogens were derived from the same maternal genotype as cyclical parthenogens. Obligate parthenogens had similar fitness compared with cyclical parthenogens in terms of the intrinsic rate of increase (calculated from life tables). However, population growth of cyclical parthenogens was predicted to be much lower: sexual female offspring do not contribute to immediate population growth in Brachionus, since they produce either males or diapausing eggs. Hence, if cyclical parthenogens constantly produce a high proportion of sexual offspring, there is a cost of sex, and obligate parthenogens can invade. This prediction was confirmed in laboratory competition experiments.     

Mixed substrate-metabolism in an obligate methanol utilizer: chemostat studies

In Pseudomonas C, an obligate RMP-methylotroph, externally added formic acid and multi-carbon intermediates are co-metabolized in the obligate presence of methanol. Cell yield and methanol-carbon conversion to cell mass are optimal in a chemostat culture growing on a mixture of energy sources and methanol as the sole limiting carbon source. Growth on methanol as the sole, obligate energy source and an additional carbon source (e.g. pyruvate) is less efficient. Under these energy limited conditions, the cyclic oxidation pathway is predominantly operated.     

Periodic solutions in a model of competition between plasmid-bearing and plasmid-free organisms in a chemostat with an inhibitor

We obtain necessary and sufficient conditions on the existence of a unique positive equilibrium point and a set of sufficient conditions on the existence of periodic solutions for a 3-dimensional system which arises from a model of competition between plasmid-bearing and plasmid-free organisms in a chemostat with an inhibitor. Our results improve the corresponding results obtained by Hsu, Luo, and Waltman [1]. Received: 20 November 1997 / Revised version: 12 February 1999 / Published online: 20 December 2000     

Global stability of obligate mutualism in community modules with facultative mutualists

Mutualism is a fundamental building block of ecological communities and an important driver of biotic evolution. Classic theory suggests that a pairwise two‐species obligate mutualism is fragile, with a large perturbation potentially driving both mutualist populations into extinction. In nature, however, there are many cases of pairwise obligate mutualism. Such pairwise obligate mutualisms are occasionally associated with additional interactions with facultative mutualists. Here, we use a mathematical model to show that when a two‐species obligate mutualism has a single additional link to a third facultative mutualist, the obligate mutualism can become permanently persistent. In the model, a facultative mutualist interacts with one of two inter‐dependent obligate mutualists, and the facultative mutualist enhances the persistence not only of its directly interacting obligate mutualist, but also that of the other obligate mutualist indirectly, enabling the permanent coexistence of the three mutualist species. The effect of the facultative mutualist is strong; it can allow a three‐species permanent coexistence even when two obligate mutualists by themselves are not sustainable (i.e. not locally stable). These results suggest that facultative mutualists can play a pivotal role for the persistence of obligate mutualisms, and contribute to a better understanding on the mechanisms maintaining more complex mutualistic networks of multiple species.     

Repeated independent evolution of obligate pollination mutualism in the Phyllantheae-Epicephala association

The well-known fig-fig wasp and yucca-yucca moth mutualisms are classic examples of obligate mutualisms that have been shaped by millions of years of coevolution. Pollination systems involving obligate seed parasites are only expected to evolve under rare circumstances where their positive effects are not swamped by abundant co-pollinators and heavy costs resulting from seed destruction. Here, we show that, in Phyllantheae, specialization to pollination by Epicephala moths evolved at least five times, involving more than 500 Phyllantheae species in this obligate association. Active pollination behaviour evolved once in Epicephala, 10-20 Myr after the initial divergence of their host plants. The pollinating Epicephala moths thus radiated on an already-diverged host lineage and successively colonized new Phyllantheae hosts, thereby giving rise to repeated independent evolution of the specialized pollination system in Phyllantheae. The present evolutionary success of this association rests entirely upon active pollination by Epicephala, making this a distinct example of an evolutionary key innovation. Overall, our findings provide a clear empirical demonstration of how a combination of evolutionary innovation and partner shifts facilitates the spread of mutualism in a coevolving species interaction.     

No evidence for a Ganoderma spore dispersal mutualism in an obligate spore-feeding beetle Zearagytodes maculifer

The role of spore dispersal mutualism remains equivocal in many fungus-insect assemblages. We tested experimentally whether an obligate spore-feeding beetle Zearagytodes maculifer has a mutualistic relationship with its host bracket fungus Ganoderma cf. applanatum via spore dispersal. We asked three specific questions: (1) whether or not Ganoderma spore germination rate is increased via beetle digestive activity and (2) is dependent on temperature and sporocarp identity. Spore germination rates were examined in 2×3×2 factorial experiments (spores consumed by beetles or not×temperature 20, 25, and 30°C×two independent pairs of sporocarp-beetle populations) replicated five times in an array of 60 experimental cultures. Analysis showed that consumption by beetles significantly reduced germination rate of Ganoderma spores. The effect of temperature was modulated by the effect of individual sporocarp, and was overridden by beetle feeding. Microscopic analysis revealed that spores from beetle faecal pellets exhibited extensive damage to their thin outer walls (pellicles) and thick inner walls, as well as significant loss of cytoplasm, while control spores were intact. The overall evidence argued against our spore dispersal mutualism hypothesis, suggesting that Z. maculifer can potentially exert a negative, if vanishingly small, fitness effect on its host fungus G. cf. applanatum.     

Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae)

The landmark discovery of obligate pollination mutualism between Glochidion plants and Epicephala moths has sparked increased interest in the pollination systems of Phyllantheae plants. In this paper I review current information on the natural history and evolutionary history of obligate pollination mutualism in Phyllantheae. Currently, an estimated >500 species are mutualistic with Epicephala moths that actively pollinate flowers and whose progeny feed on the resulting seeds. The Phyllantheae also includes species that are not mutualistic with Epicephala moths and are instead pollinated by bees and/or flies or ants. Phylogenetic analyses indicate that the mutualism evolved independently five times within Phyllantheae, whereas active pollination behavior, a key innovation in this mutualism, evolved once in Epicephala . Reversal of mutualism has occurred at least once in both partner lineages, involving a Breynia species that evolved an alternative pollination system and a derived clade of Epicephala that colonized ant-pollinated Phyllantheae hosts and thereby lost the pollinating habit. The plant–moth association is highly species specific, although a strict one-to-one assumption is not perfectly met. A comparison of plant and moth phylogenies suggests signs of parallel speciation, but partner switches have occurred repeatedly at a range of taxonomic levels. Overall, the remarkable species diversity and multiple originations of the mutualism provide excellent opportunities to address many important questions on mutualism and the coevolutionary process. Although research on the biology of the mutualism is still in its infancy, the Phyllantheae– Epicephala association holds promise as a new model system in ecology and evolutionary biology.     

Evolution of obligate pollination mutualism in New Caledonian Phyllanthus (Euphorbiaceae)

About half a dozen obligate pollination mutualisms between plants and their seed-consuming pollinators are currently recognized, including fig-fig wasp, yucca-yucca moth, and the recently discovered Glochidion tree-Epicephala moth mutualisms. A common principle among these interactions is that the pollinators consume only a limited amount of the seed crop within a developing fruit (or fig in the case of fig-fig wasp mutualism), thereby ensuring a net benefit to plant reproduction. A novel obligate, seed-parasitic pollination mutualism between two species of New Caledonian Phyllanthus (Euphorbiaceae), a close relative of Glochidion, and Epicephala moths (Gracillariidae) is an exception to this principle. The highly specialized flowers of Phyllanthus are actively and exclusively pollinated by species-specific Epicephala moths, whose larvae consume all six ovules of the developing fruit. Some flowers pollinated by the moths remain untouched, and thus a fraction of the fruits is left intact. Additional evidence for a similar association of Epicephala moths in other Phyllanthus species suggests that this interaction is a coevolved, species-specific pollination mutualism. Implications for the evolutionary stability of the system, as well as differences in mode of interaction with respect to the Glochidion-Epicephala mutualism, are discussed.     

Florivore impacts on plant reproductive success and pollinator mortality in an obligate pollination mutualism

Florivores are present in many pollination systems and can have direct and indirect effects on both plants and pollinators. Although the impact of florivores are commonly examined in facultative pollination mutualisms, their effects on obligate mutualism remain relatively unstudied. Here, we used experimental manipulations and surveys of naturally occurring plants to assess the effect of florivory on the obligate pollination mutualism between yuccas and yucca moths. Yucca filamentosa (Agavaceae) is pollinated by the moth Tegeticula cassandra (Lepidoptera: Prodoxidae), and the mutualism also attracts two florivores: a generalist, the leaf-footed bug Leptoglossus phyllopus (Hemiptera: Coreidae), and a specialist, the beetle Hymenorus densus (Coleoptera: Tenebrionidae). Experimental manipulations of leaf-footed bug densities on side branches of Y. filamentosa inflorescences demonstrated that feeding causes floral abscission but does not reduce pollen or seed production in the remaining flowers. Similar to the leaf-footed bugs, experimental manipulations of beetle densities within individual flowers demonstrated that beetle feeding also causes floral abscission, but, in addition, the beetles also cause a significant reduction in pollen availability. Path analyses of phenotypic selection based on surveys of naturally occurring plants revealed temporal variation in the plant traits important to plant fitness and the effects of the florivores on fitness. Leaf-footed bugs negatively impacted fitness when fewer plants were flowering and leaf-footed bug density was high, whereas beetles had a positive effect on fitness when there were many plants flowering and their densities were low. This positive effect was likely due to adult beetles consuming yucca moth eggs while having a negligible effect on floral abscission. Together, the actions of both florivores either augmented the relationship of plant traits and fitness or slightly weakened the relationship. Overall, the results suggest that, although florivores are always present during flowering, the impact of florivores on phenotypic selection in yuccas is strongly mitigated by changes in their densities on plants from year to year. In contrast, both florivores consistently influenced pollinator larval mortality through floral abscission, and H. densus beetles additionally via the consumption of pollinator eggs.     

Global dynamics of a chemostat competition model with distributed delay

 We study the global dynamics of n-species competition in a chemostat with distributed delay describing the time-lag involved in the conversion of nutrient to viable biomass. The delay phenomenon is modelled by the gamma distribution. The linear chain trick and a fluctuation lemma are applied to obtain the global limiting behavior of the model. When each population can survive if it is cultured alone, we prove that at most one competitor survives. The winner is the population that has the smallest delayed break-even concentration, provided that the orders of the delay kernels are large and the mean delays modified to include the washout rate (which we call the virtual mean delays) are bounded and close to each other, or the delay kernels modified to include the washout factor (which we call the virtual delay kernels) are close in L ¹-norm. Also, when the virtual mean delays are relatively small, it is shown that the predictions of the distributed delay model are identical with the predictions of the corresponding ODEs model without delay. However, since the delayed break-even concentrations are functions of the parameters appearing in the delay kernels, if the delays are sufficiently large, the prediction of which competitor survives, given by the ODEs model, can differ from that given by the delay model. Received: 9 August 1997 / Revised version: 2 July 1998     

Pollinator attraction to volatiles from virgin and pollinated host flowers in a yucca/moth obligate mutualism

The classic obligate pollination–seed consumption mutualism between yuccas and yucca moths has been thought to be mediated by chemical cues, but empirical data on pollinator attraction to host floral volatiles in this association have been lacking. Here we show that the scent from virgin flowers of the host Yucca glauca is sufficient to attract its obligate pollinator Tegeticula yuccasella in Y‐tube olfactometer tests. Interestingly, both sexes of moths were attracted to the scent stimulus. Because yucca moths mate inside host flowers, the attraction of both females and males to host floral volatiles is likely to increase encounter rates. In a second test, female moths did not discriminate between virgin and hand‐pollinated flowers, indicating no post‐pollination change in scent production by the host that would lead to a reduction in pollinator attraction and thereby limit exploitation of the available seeds in host flowers. However, other mechanisms that could stabilise the mutualism between T. yuccasella and its yucca hosts have already been documented, i.e. selective abortion of heavily infested flowers, and a female‐derived host‐marking pheromone. Headspace collection and GC–MS were used to identify the blend of floral volatiles emitted by Y. glauca, which was found to be very similar to those of two other allopatric capsular‐fruited species, Y. elata and Y. filamentosa, revealing strong conservation of this trait within Yucca section Chaenocarpa.     

Anomalous,extreme weather disrupts obligate seed dispersal mutualism: snow in a subtropical forest ecosystem

Ongoing global climate change is predicted to increase the frequency and magnitude of extreme weather events, impacting population dynamics and community structure. There is, however, a critical lack of case studies considering how climatic perturbations affect biotic interactions. Here, we document how an obligate seed dispersal mutualism was disrupted by a temporally anomalous and meteorologically extreme interlude of unseasonably frigid weather, with accompanying snowstorms, in subtropical China, during January–February 2008. Based on the analysis of 5892 fecal samples (representing six mammalian seed dispersers), this event caused a substantial disruption to the relative seed dispersal function for the raisin tree Hovenia dulcis from prestorm 6.29 (2006) and 11.47 (2007), down to 0.35 during the storm (2008). Crucially, this was due to impacts on mammalian seed dispersers and not due to a paucity of fruit, where 4.63 fruit per branch were available in January 2008, vs. 3.73 in 2006 and 3.58 in 2007. An induced dietary shift occurred among omnivorous carnivores during this event, from the consumption fruit to small mammals and birds, reducing their role in seed dispersal substantially. Induced range shift extinguished the functionality of herbivorous mammals completely, however, seed dispersal function was compensated in part by three omnivorous carnivores during poststorm years, and thus while the mutualism remained intact it was enacted by a narrower assemblage of species, rendering the system more vulnerable to extrinsic perturbations. The storm's extended effects also had anthropogenic corollaries – migrating ungulates becoming exposed to heightened levels of illegal hunting – causing long‐term modification to the seed dispersal community and mutualism dynamics. Furthermore, degraded forests proved especially vulnerable to the storm's effects. Considering increasing climate variability and anthropogenic disturbance, the impacts of such massive, aberrant events warrant conservation concern, while affording unique insights into the stability of mutualisms and the processes that structure biodiversity and mediate ecosystem dynamics.