Cheating and the evolutionary stability of mutualisms

Interspecific mutualisms have been playing a central role in the functioning of all ecosystems since the early history of life. Yet the theory of coevolution of mutualists is virtually nonexistent, by contrast with well-developed coevolutionary theories of competition, predator–prey and host–parasite interactions. This has prevented resolution of a basic puzzle posed by mutualisms: their persistence in spite of apparent evolutionary instability. The selective advantage of 'cheating', that is, reaping mutualistic benefits while providing fewer commodities to the partner species, is commonly believed to erode a mutualistic interaction, leading to its dissolution or reciprocal extinction. However, recent empirical findings indicate that stable associations of mutualists and cheaters have existed over long evolutionary periods. Here, we show that asymmetrical competition within species for the commodities offered by mutualistic partners provides a simple and testable ecological mechanism that can account for the long-term persistence of mutualisms. Cheating, in effect, establishes a background against which better mutualists can display any competitive superiority. This can lead to the coexistence and divergence of mutualist and cheater phenotypes, as well as to the coexistence of ecologically similar, but unrelated mutualists and cheaters

Gelechiidae Moths Are Capable of Chemically Dissolving the Pollen of Their Host Plants

Background: Many insects feed on pollen surface lipids and contents accessible through the germination pores. Pollen walls, however, are not broken down because they consist of sporopollenin and are highly resistant to physical and enzymatic damage. Here we report that certain Microlepidoptera chemically dissolve pollen grains with exudates from their mouthparts. Methodology/Principal Findings: Field observations and experiments in tropical China revealed that two species of Deltophora (Gelechioidea) are the exclusive pollinators of two species of Phyllanthus (Phyllanthaceae) on which their larvae develop and from which the adults take pollen and nectar. DNA sequences placed the moths and plants phylogenetically and confirmed that larvae were those of the pollinating moths; molecular clock dating suggests that the moth clade is younger than the plant clade. Captive moths with pollen on their mouthparts after 2-3 days of starvation no longer carried intact grains, and SEM photographs showed exine fragments on their proboscises. GC-MS revealed cis-b-ocimene as the dominant volatile in leaves and flowers, but GC-MS analyses of proboscis extracts failed to reveal an obvious sporopollenindissolving compound. A candidate is ethanolamine, which occurs in insect hemolymphs and is used to dissolve sporopollenin by palynologists. Conclusions/Significance: This is the first report of any insect and indeed any animal chemically dissolving pollen

Presence of fruits decreases probability of retaining flowers in a sequentially flowering plant

Both intrinsic and extrinsic plant processes affect the fate of flowers along an inflorescence in sequentially flowering plants. We investigated whether the intrinsic process of competition for limited resource between fruits and flowers owing to resource preemption or sink strength of basal fruits, or architectural effects due to posi- tional differences in the probability of retaining flowers, explains a lower probability of retaining distal flowers inYucca glauca. Further, we investigated how the extrinsic process of seed herbivory interacts with the plant’s intrinsic processes of flower retention. We carried out a field experiment to compare flower retention among nine combi- nations of three inflorescence treatments (basal flowers only, distal flowers only, distal flowers with presence of basal fruits) and three ovule damage treatments (no, low and high) that serve as a cue for potential future seed herbivory. Also, we quantified flower retention in naturally pollinated inflorescences. Experimental results showed that the probabilities of retaining basal and distal flowers in the absence of basal fruits were similar, thus rejecting the architectural effects hypothesis. Further, in the presence of basal fruits that were in their initial stages of growth, the probability of retaining distal flowers decreased, which supports the sink strength hypothesis. We did not see an effect of ovule damage. In naturally pollinated inflorescences, the probability of retaining distal flowers decreased with increasing number of basal fruits. Results suggest that basal fruits constitute strong resource sinks reducing the probability of retaining distal flowers. Previous studies have tested this mechanism in cultivated plants. Our study shows evidence for this mechanism in a wild flower population

Replicated host-race formation in bogus yucca moths: genetic and ecological divergence of Prodoxus quinquepunctellus on yucca hosts

Goal: Assess host-race formation in certain moths by examining their genetic and ecological differentiation. Organisms: Stalk-feeding moths, Prodoxus quinquepunctellus, collected from sympatric populations of Yucca elata and Y rostrata in west Texas, USA. Results: Moths on the two yuccas differed significantly in mtDNA haplotype frequencies, emergence time, wing dot number, body size, and ovipositor size and shape. Conclusion: Host-race formation has probably occurred in this yucca moth although genetic divergence was low

CONDITION-DEPENDENT LIFE HISTORY STRATEGIES

Many organisms evolve condition-dependent life history strategies to maximize their lifetime fitness in response to intrinsic and extrinsic processes. I investigated a sequentially flowering plant’s strategy to allocate resources to retain flowers versus grow existing basal fruits to a larger size, using the plant Yucca glauca. The sink strength hypothesis suggests basal fruits are nutrient sinks depriving distal flowers of resources and reducing their probability of retention. A low probability of retention of distal flowers can also be explained by the architectural effects hypothesis. This hypothesis posits inherent positional differences in structures along an inflorescence such as flower size and amount of vascular tissues decrease flower retention with increasing flower position, independent of the number of basal fruits. I experimentally showed that the presence of basal fruits decreased the probability of retention of distal flowers, which supports the sink strength hypothesis. Further, in the absence of fruits, plants retained distal flowers at a probability similar to that of basal flowers, which is inconsistent with the architectural effects hypothesis. Next, I developed a stochastic dynamic programming model to examine the conditions under which decreasing flower retention in response to existing basal fruits is optimal for sequentially flowering plants. The model predicts that plants should decrease flower retention with increasing number of basal fruits when large fruits produce more viable seeds than small fruits (fruit size-dependent viability benefit). Finally, I tested if a higher probability of flower abortion in the presence of basal fruits affects the life history strategy of insects that lay eggs in flowers. Yucca glauca flowers are egg-laying sites for seed-eating insect Tegeticula yuccasella. Flowers that have a high probability of being aborted are low quality egg-laying sites for T. yuccasella because all eggs in aborted flowers die. I experimentally showed that when basal fruits were present, T. yuccasella were less likely to lay eggs in flowers. These investigations help identify mechanisms underlying condition-dependent plant and animal life history strategies that contribute to intra-population variation in life history strategies. Adviser: Brigitte Tenhumber

Comparative Phylogeography of a Coevolved Community: Concerted Population Expansions in Joshua Trees and Four Yucca Moths

Comparative phylogeographic studies have had mixed success in identifying common phylogeographic patterns among co-distributed organisms. Whereas some have found broadly similar patterns across a diverse array of taxa, others have found that the histories of different species are more idiosyncratic than congruent. The variation in the results of comparative phylogeographic studies could indicate that the extent to which sympatrically-distributed organisms share common biogeographic histories varies depending on the strength and specificity of ecological interactions between them. To test this hypothesis, we examined demographic and phylogeographic patterns in a highly specialized, coevolved community – Joshua trees (Yucca brevifolia) and their associated yucca moths. This tightly-integrated, mutually interdependent community is known to have experienced significant range changes at the end of the last glacial period, so there is a strong a priori expectation that these organisms will show common signatures of demographic and distributional changes over time. Using a database of >5000 GPS records for Joshua trees, and multi-locus DNA sequence data from the Joshua tree and four species of yucca moth, we combined paleaodistribution modeling with coalescent-based analyses of demographic and phylgeographic history. We extensively evaluated the power of our methods to infer past population size and distributional changes by evaluating the effect of different inference procedures on our results, comparing our palaeodistribution models to Pleistocene-aged packrat midden records, and simulating DNA sequence data under a variety of alternative demographic histories. Together the results indicate that these organisms have shared a common history of population expansion, and that these expansions were broadly coincident in time. However, contrary to our expectations, none of our analyses indicated significant range or population size reductions at the end of the last glacial period, and the inferred demographic changes substantially predate Holocene climate changes

The Ecology of Fine-Scale, Tissue-Specific Floral Scent Patterns in an Obligate Brood-Pollination Mutualism.

Abstract: Interactions between plants and insect pollinators are of critical importance as the majority of flowering plants rely on animals for pollination and insects are the most diverse group of pollinators on Earth. To obtain pollination services plants must attract pollinators by signaling the presence of rewards, and chemosensory cues including floral scent are of particular importance to pollinator attraction. In highly-specialized brood-pollination mutualisms, like the yucca-yucca moth mutualism, the “reward” for pollinators is a brood site and food source for their offspring: fertilized plant ovules. Being able to distinguish among floral parts is critical for yucca moths to successfully execute the complex behaviors required for oviposition and pollination. Fine-scale, tissue-specific patterns of floral scent potentially play an important role in helping pollinators to navigate toward rewards, but such patterns and their ecological consequences remain poorly understood. To address this, I examined the floral scent of the tepals and pistils of five species of Yucca. All five species of Yucca had tissue-specific patterns of scent emission. Tissue-specific patterns of floral scent also varied among Yucca species, with two species Y. reverchonii and Y. rupicola producing low to nonexistent levels of a subset of compounds of known biological relevance to pollinating moths. I also observed a trend in the oviposition behavior of the common pollinator of these five species (Tegeticula yuccasella), wherein moths oviposited at higher rates in chemically similar yuccas and at lower rates in yuccas with reduced (or no) expression of known, biologically relevant compounds. Even though there is variation in the scent profile of tepals and pistils across Yucca species, T. yuccasella successfully uses all hosts in the wild. Our results show that moths may be using a broader, potentially redundant suite of compounds to identify yuccas and their specific tissues rather than relying on a few major compounds to determine host suitability