Parasitism to mutualism continuum for Joshua trees inoculated with different communities of arbuscular mycorrhizal fungi from a desert elevation gradient.

Most desert plants form symbiotic relationships with arbuscular mycorrhizal fungi (AMF), yet fungal identity and impacts on host plants remain largely unknown. Despite widespread recognition of the importance of AMF relationships for plant functioning, we do not know how fungal community structure changes across a desert climate gradient, nor the impacts of different fungal communities on host plant species. Because climate change can shape the distribution of species through effects on species interactions, knowing how the ranges of symbiotic partners are geographically structured and the outcomes of those species interactions informs theory and improves management recommendations. Here we used high throughput sequencing to examine the AMF community of Joshua trees along a climate gradient in Joshua Tree National Park. We then used a range of performance measures and abiotic factors to evaluate how different AMF communities may affect Joshua tree fitness. We found that fungal communities change with elevation resulting in a spectrum of interaction outcomes from mutualism to parasitism that changed with the developmental stage of the plant. Nutrient accumulation and the mycorrhizal growth response of Joshua tree seedlings inoculated with fungi from the lowest (warmest) elevations was first negative, but after 9 months had surpassed that of plants with other fungal treatments. This indicates that low elevation fungi are costly for the plant to initiate symbiosis, yet confer benefits over time. The strong relationship between AMF community and plant growth suggests that variation in AMF community may have long term consequences for plant populations along an elevation gradient.

The Bear Giant-Skipper genome suggests genetic adaptations to living inside yucca roots.

Giant-Skippers (Megathymini) are unusual thick-bodied, moth-like butterflies whose caterpillars feed inside Yucca roots and Agave leaves. Giant-Skippers are attributed to the subfamily Hesperiinae and they are endemic to southern and mostly desert regions of the North American continent. To shed light on the genotypic determinants of their unusual phenotypic traits, we sequenced and annotated a draft genome of the largest Giant-Skipper species, the Bear (Megathymus ursus violae). The Bear skipper genome is the least heterozygous among sequenced Lepidoptera genomes, possibly due to much smaller population size and extensive inbreeding. Their lower heterozygosity helped us to obtain a high-quality genome with an N50 of 4.2 Mbp. The ~ 430 Mb genome encodes about 14000 proteins. Phylogenetic analysis supports placement of Giant-Skippers with Grass-Skippers (Hesperiinae). We find that proteins involved in odorant and taste sensing as well as in oxidative reactions have diverged significantly in Megathymus as compared to Lerema, another Grass-Skipper. In addition, the Giant-Skipper has lost several odorant and gustatory receptors and possesses many fewer (1/3-1/2 of other skippers) anti-oxidative enzymes. Such differences may be related to the unusual life style of Giant-Skippers: they do not feed as adults, and their caterpillars feed inside Yuccas and Agaves, which provide a source of antioxidants such as polyphenols.

Morphological and molecular characterization of a new succulenticolous Physarum (Myxomycetes, Amoebozoa) with unique polygonal spores linked in chains.

A new plasmodiocarpic and sporocarpic species of myxomycete in the genus Physarum is described and illustrated. This new species appeared on decayed leaves and remains of succulent plants (Agave, Opuntia, Yucca) growing in arid zones. It differs from all other species in the genus in having polyhedral spores linked in chains like a string of beads, a unique feature within all known myxomycetes. Apart from detailed morphological data, partial sequences of both the small-subunit ribosomal RNA and elongation factor 1-alpha genes, generated from four isolates collected in two distant regions, i.e., Mexico and Canary Islands, are also provided in this study. Combined evidence supports the identity of the specimens under study as a new species.

Yucca brevifolia fruit production, predispersal seed predation, and fruit removal by rodents during two years of contrasting reproduction.

PREMISE OF THE STUDY: The distribution of Yucca brevifolia, a keystone species of the Mojave Desert, may contract with climate change, yet reproduction and dispersal are poorly understood. We tracked reproduction, seed predation, and fruit dispersal for two years and discuss whether Y. brevifolia is a masting species. METHODS: Fruit maturation, seed predation (larval yucca moths), and fruit dispersal (rodents) were monitored on a random sample of panicles during 2013 and 2014, which were years of high and low reproduction, respectively. Fates of fruits placed on the ground and in canopies were also tracked. Rodents were live-trapped to assess abundance and species composition. KEY RESULTS: In 2013, 66% of inflorescences produced fruit of which 53% escaped larval predation; 19.5% of seeds were destroyed in infested fruits. Total seed production was estimated to be >100 times greater in 2013 than 2014. One-third of the fruit crop fell to the ground and was removed by rodents over the course of 120 d. After ground fruits became scarce, rodents exploited canopy fruits. Rodent numbers were low in 2013, so fruits remained in canopies for 370 d. In 2014, fruit production was approximately 20% lower. Larvae infested the majority of fruits, and almost twice the number of seeds were damaged. Fruits were exploited by rodents within 65 d. CONCLUSIONS: High fertilization, prolific seed production, and low predispersal predation in 2013 suggests that pollinator attraction and satiation of seed predators influence masting in Y. brevifolia. Abundant, prolonged fruit availability to seed-dispersing rodents likely extends recruitment opportunities during mast years.

The roles of geography and founder effects in promoting host-associated differentiation in the generalist bogus yucca moth Prodoxus decipiens.

There is ample evidence that host shifts in plant-feeding insects have been instrumental in generating the enormous diversity of insects. Changes in host use can cause host-associated differentiation (HAD) among populations that may lead to reproductive isolation and eventual speciation. The importance of geography in facilitating this process remains controversial. We examined the geographic context of HAD in the wide-ranging generalist yucca moth Prodoxus decipiens. Previous work demonstrated HAD among sympatric moth populations feeding on two different Yucca species occurring on the barrier islands of North Carolina, USA. We assessed the genetic structure of P. decipiens across its entire geographic and host range to determine whether HAD is widespread in this generalist herbivore. Population genetic analyses of microsatellite and mtDNA sequence data across the entire range showed genetic structuring with respect to host use and geography. In particular, genetic differentiation was relatively strong between mainland populations and those on the barrier islands of North Carolina. Finer scale analyses, however, among sympatric populations using different host plant species only showed significant clustering based on host use for populations on the barrier islands. Mainland populations did not form population clusters based on host plant use. Reduced genetic diversity in the barrier island populations, especially on the derived host, suggests that founder effects may have been instrumental in facilitating HAD. In general, results suggest that the interplay of local adaptation, geography and demography can determine the tempo of HAD. We argue that future studies should include comprehensive surveys across a wide range of environmental and geographic conditions to elucidate the contribution of various processes to HAD.

Shift in egg-laying strategy to avoid plant defense leads to reproductive isolation in mutualistic and cheating yucca moths.

Through the process of ecological speciation, insect populations that adapt to new host plant species or to different plant tissues could speciate if such adaptations cause reproductive isolation. One of the key issues in this process is identifying the mechanisms by which adaptation in ecological traits leads directly to reproductive isolation. Here I show that within a radiation of specialist moths that pollinate and feed on yuccas, shifts in egg placement resulted in changes in female moth egg-laying structures that led to concomitant changes in male reproductive morphology. As pollinator moths evolved to circumvent the ability of yuccas to selectively abscise flowers that contain pollinator eggs, ovipositor length became shorter. Because mating occurs through the ovipositor, shortening of the ovipositor also led to significantly shorter and wider male intromittent organs. In instances where two pollinator moth species occur in sympatry and on the same host plant species, there is one short and one long ovipositor species that are reproductively isolated. Given that many plant-feeding insects lay eggs into plant tissues, changes in ovipositor morphology that lead to correlated changes in reproductive morphology may be a mechanism that maintains reproductive isolation among closely related species using the same host plant species.

Mutualism favours higher host specificity than does antagonism in plant-herbivore interaction.

Coevolved mutualisms often exhibit high levels of partner specificity. Obligate pollination mutualisms, such as the fig-fig wasp and yucca-yucca moth systems, represent remarkable examples of such highly species-specific associations; however, the evolutionary processes underlying these patterns are poorly understood. The prevailing hypothesis suggests that the high degree of specificity in pollinating seed parasites is the fortuitous result of specialization in their ancestors because these insects are derived from endophytic herbivores that are themselves highly host-specific. Conversely, we show that in the Glochidion-Epicephala obligate pollination mutualism, pollinators are more host-specific than are closely related endophytic leaf-feeding taxa, which co-occur with Epicephala on the same Glochidion hosts. This difference is probably not because of shifts in larval diet (i.e. from leaf- to seed-feeding), because seed-eating lepidopterans other than Epicephala do not show the same degree of host specificity as Epicephala. Species of a tentative sister group of Epicephala each attack several distantly related plants, suggesting that the evolution of strict host specificity is tied to the evolution of pollinator habit. These results suggest that mutualists can attain higher host specificity than that of their parasitic ancestors and that coevolutionary selection can be a strong promoter of extreme reciprocal specialization in mutualisms.

Host-associated divergence and incipient speciation in the yucca moth Prodoxus coloradensis (Lepidoptera: Prodoxidae) on three species of host plants.

A wide range of evolutionary processes have been implicated in the diversification of yuccas and yucca moths, which exhibit ecological relationships that extend from obligate plant-pollinator mutualisms to commensalist herbivory. Prodoxus coloradensis (Lepidoptera: Prodoxidae) is a yucca moth, which feeds on the flowering stalks of three Yucca species as larvae, but does not provide pollination service. To test for evidence of host-associated speciation, we examined the genetic structure of P. coloradensis using mitochondrial (cytochrome oxidase I) and nuclear (elongation factor 1 alpha) DNA sequence data. Multilocus coalescent simulations indicate that moths on different host plant species are characterized by recent divergence and low levels of effective migration, with large effective population sizes and considerable retention of shared ancestral polymorphism. Although geographical distance explains a proportion of the mitochondrial and nuclear DNA variation among moths on different species of Yucca, the effect of host specificity on genetic distance remains significant after accounting for spatial isolation. The results of this study indicate that differentiation within P. coloradensis is consistent with the evolution of incipient species affiliated with different host plants, potentially influenced by sex-biased dispersal and female philopatry.

Host plant selection, larval survival, and reproductive phenology in Megathymus yuccae (Lepidoptera: Hesperiidae).

Our primary objective in this study was to determine the plant level and environmental factors that affect oviposition choice and subsequent offspring survival in Megathymus yuccae (Boisduval and Leconte) on its host plant, Yucca filamentosa L. A preliminary survey suggested that the frequency of pupal eclosion tent presence increased only with host plant height. In an expanded survey conducted during the adult flight period the following spring, we found that plant height increased the probability of oviposition, whereas the density of herbaceous stems and fire damage decreased the probability of egg presence. Similarly, the number of eggs on occupied plants increased with plant height and decreased with fire damage. When we surveyed the plants from the spring 2008 sampling the following winter to determine presence of late-instar larvae or pupae, we found that the probability that at least one larva survived on previously occupied plants decreased with the density of herbaceous stems. These results collectively suggest that larger, unburned Y. filamentosa individuals and those in relatively open areas are more attractive as host plants for oviposition and that larval performance is generally, but not exclusively, consistent with female preference in this system.

Aerial reproductive structures of vascular plants as a microhabitat for myxomycetes.

This study explored the occurrence and distribution of myxomycete species on the aerial reproductive structures of vascular plants. Eight species of vascular plants representing five families were sampled. The doubled rope climbing method was used to collect bark and cones from the canopy of Pinus echinata. Bark and aerial seed pods were gathered from Cercis canadensis, follicles and stems from Asclepias syriaca, dried composite inflorescences and stems from Echinacea angustifolia, E. pallida, and E. paradoxa var. paradoxa, and capsules and stems from Yucca glauca and Y. smalliana. Reproductive structures and bark/stems for 202 host plants were separated and cultured in 541 moist chambers, resulting in 118 collections yielding 32 myxomycete species representing 11 genera, seven families and five orders. There was no significant difference in pH values of the reproductive structures and bark/stems of the host plants, however legume pods of C. canadensis (6.9 +/- 1.3) had higher pH than the bark (6.0 +/- 1.1) and had a different composition of myxomycete species. Myxomycete orders have optimal pH ranges. Nonmetric multidimensional scaling, multiresponse permutation procedure and indicator species analysis showed a significant difference in species richness of reproductive structures and bark/stems. The bark of trees had greater mean species richness of myxomycetes than the reproductive structures, but the reproductive structures of herbaceous plants had greater mean species richness of myxomycetes than the stems. A new term, herbicolous myxomycetes, is proposed for a group of myxomycetes frequently associated with herbaceous, perennial, grassland plants. An undescribed species of Arcyria occurred only on cones of P. echinata.