Judith X. Becerra

COMPETITION-DEPENDENT ABSCISSION OF SELF-POLLINATED FLOWERS OF PHORMIUM TENAX (AGAVACEAE): A SECOND ACTION OF SELF-INCOMPATIBILITY AT THE WHOLE FLOWER LEVEL?

The relative success of fruit from paired self‐ and cross‐pollinations was examined in Phormium tenax when the contrasted pollinations were separated by different distances on the same and different inflorescences. We determined whether the retention of selfed fruits differed from that of crossed fruits and whether it depended on the level of competition with crossed fruit, the number of seeds per fruit, and/or the presence of earlier developing fruit. We found that the success of selfed fruits is determined by the degree of competition with crossed fruits and may be an expression of self‐incompatibility. Competition‐dependence of the abscission of selfed flowers has not been documented previously. It is parallel to cryptic self‐incompatibility in which individual self‐pollen grains are not as successful as cross‐pollen when competing on the same pistil. The competition‐dependent abscission of self‐pollinations considered here, however, operates at the level of whole flowers. The phenomenon of competition‐dependent abscission of selfed flowers in P. tenax also has implications for the measurement and interpretation of self‐incompatibility in other species. Self‐incompatibility is a quantitative phenomenon. The facultative success of selfing shows that the effective strength of self‐incompatibility can be highly susceptible to the conditions of competition under which it is measured. The competition‐dependent abscission of selfed flowers allows a high level of outcrossing to be achieved while it assures seed set when pollinations are scarce. Several other causes of intermediate selfing frequencies can also be explained by this “best‐of‐both‐worlds” hypothesis.

The impact of herbivore–plant coevolution on plant community structure

Coevolutionary theory proposes that the diversity of chemical structures found in plants is, in large part, the result of selection by herbivores. Because herbivores often feed on chemically similar plants, they should impose selective pressures on plants to diverge chemically or bias community assembly toward chemical divergence. Using a coevolved interaction between a group of chrysomelid beetles and their host plants, I tested whether coexisting plants of the Mexican tropical dry forest tend to be chemically more dissimilar than random. Results show that some of the communities are chemically overdispersed and that overdispersion is related to the tightness of the interaction between plants and herbivores and the spatial scale at which communities are measured. As coevolutionary specialization increases and spatial scale decreases, communities tend to be more chemically dissimilar. At fairly local scales and where herbivores have tight, one-to-one interactions with plants, communities have a strong pattern of chemical disparity.

Extrafloral nectaries: a defense against ant-Homoptera mutualisms?

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Parasitic wasp responses to symbiont-based defense in aphids

BackgroundRecent findings indicate that several insect lineages receive protection against particular natural enemies through infection with heritable symbionts, but little is yet known about whether enemies are able to discriminate and respond to symbiont-based defense. The pea aphid, Acyrthosiphon pisum, receives protection against the parasitic wasp, Aphidius ervi, when infected with the bacterial symbiont Hamiltonella defensa and its associated bacteriophage APSE (Acyrthosiphon pisumsecondary endosymbiont). Internally developing parasitoid wasps, such as A. ervi, use maternal and embryonic factors to create an environment suitable for developing wasps. If more than one parasitoid egg is deposited into a single aphid host (superparasitism), then additional complements of these factors may contribute to the successful development of the single parasitoid that emerges.ResultsWe performed experiments to determine if superparasitism is a tactic allowing wasps to overcome symbiont-mediated defense. We found that the deposition of two eggs into symbiont-protected aphids significantly increased rates of successful parasitism relative to singly parasitized aphids. We then conducted behavioral assays to determine whether A. ervi selectively superparasitizes H. defensa-infected aphids. In choice tests, we found that A. ervi tends to deposit a single egg in uninfected aphids, but two or more eggs in H. defensa-infected aphids, indicating that oviposition choices may be largely determined by infection status. Finally, we identified differences in the quantity of the trans-β-farnesene, the major component of aphid alarm pheromone, between H. defensa-infected and uninfected aphids, which may form the basis for discrimination.ConclusionsHere we show that the parasitic wasp A. ervi discriminates among symbiont-infected and uninfected aphids, and changes its oviposition behavior in a way that increases the likelihood of overcoming symbiont-based defense. More generally, our results indicate that natural enemies are not passive victims of defensive symbionts, and that an evolutionary arms race between A. pisum and the parasitoid A. ervi may be mediated by a bacterial symbiosis.

Nuclear ribosomal DNA phylogeny and its implications for evolutionary trends in Mexican Bursera (Burseraceae)

The genus Bursera (Burseraceae) is one of the most diversified and abundant groups of plants of the tropical dry forests of Mexico. In order to provide a basis for better understanding of its evolutionary biology, we reconstructed a phylogeny of 57 species and varieties using the nucleotide sequences of the internal transcribed spacer regions (ITS1 and ITS2) of 18S-26S and the 5.8S coding region of nuclear ribosomal DNA. We used four species of the allied genera Commiphora and Boswellia and one species of Spondias (Anacardiaceae) as outgroups. Our results support the views that Bursera is monophyletic and more closely related to Commiphora than to Boswellia. The division of Bursera into sections Bullockia and Bursera is also strongly supported by our phylogeny. Several other subclades also had high bootstrap values, especially within section Bursera. We use the phylogeny as a basis for discussing evolutionary tendencies in bark, leaves, breeding systems, and fruits.

Evolution of Mexican Bursera (Burseraceae) inferred from ITS, ETS, and 5S nuclear ribosomal DNA sequences

I reconstructed a phylogeny of 66 species and varieties of Bursera and 9 outgroup species using sequences of the internal transcribed spacer region (ITS), the 5S non-transcribed region (5S-NTS), and the external transcribed region (ETS) of nuclear ribosomal DNA. This study extends a previously proposed parsimony-based phylogenetic study that used the ITS sequences of 57 Bursera species and five outgroups. Parsimony and maximum likelihood methods were used to infer the phylogeny in this new study. Analyses of the combined data sets largely confirmed the phylogenetic relationships proposed by the previous molecular study but generated a considerably more robust topology. The new phylogenies corroborate the monophyly of the genus, and its division into the two monophyletic subgenera or sections, Bursera and Bullockia. The current analyses also identify four main groups of species in section Bursera, and two in section Bullockia, confirming some of the previously proposed groups based on fruit, flower, and leaf morphology. One previously problematic species B. sarcopoda, which has sometimes been placed in Commiphora, is shown to belong in Bursera. Another controversial species, Commiphora leptophloeos, which was thought to belong to Bursera, falls within Commiphora.

Seed dispersal of desert annuals

We quantified seed dispersal in a guild of Sonoran Desert winter desert annuals at a protected natural field site in Tucson, Arizona, USA. Seed production was suppressed under shrub canopies, in the open areas between shrubs, or both by applying an herbicide prior to seed set in large, randomly assigned removal plots (10-30 m diameter). Seedlings were censused along transects crossing the reproductive suppression borders shortly after germination. Dispersal kernels were estimated for Pectocarya recurvata and Schismus barbatus from the change in seedling densities with distance from these borders via inverse modeling. Estimated dispersal distances were short, with most seeds traveling less than a meter. The adhesive seeds of P. recurvata went farther than the small S. barbatus seeds, which have no obvious dispersal adaptation. Seeds dispersed farther downslope than upslope and farther when dispersing into open areas than when dispersing into shrubs. Dispersal distances were short relative to the pattern of spatial heterogeneity created by the shrub and open space mosaic. This suggests that dispersal could contribute to local population buildup, possibly facilitating species coexistence. Overall, these results support the hypothesis that escape in time via delayed germination is likely to be more important for desert annuals than escape in space.

Squirt-gun defense in Bursera and the chrysomelid counterploy

I determined the impact of resins canals of Bursera schlechtendalii on the growth and survival of its specialized vein—cutting beetle Blepharida sp. nov. Bursera schlechtendalii produces terpenes stored under pressure in networks of canals that run throughout the cortex of stem and in the leaves. When a leaf is broken, it releases abundant resins, which may bathe the leaf surface and often form a squirt that travels for up to 150 cm. Plants vary in the proportion of their leaves that release resins after damage. Larvae of the chrysomelid genus Blepharida can inflict substantial damage to plants because they avoid the squirt response by cutting the leaf veins before consuming the leaves. Nevertheless, resins still protect plants against this insect. Both naturally occurring and experimentally placed larvae had higher mortality on highly responsive plants. Young larvae became mired in secretions after rupturing the canals and died. Also, on highly responsive plants larvae spent more time cutting veins and grew more slowly. Thus, while the squirt response of Bursera is not a completely effective defense, it imposes a handling—time cost on larvae, reduces their growth rate, and increases their mortality.

Seed morphometrics and adaptive geographic differentiation

Adaptive geographic differentiation is documented for seed morphology of 36 populations of Heterosperma pinnatum Cav. (Asteraceae), a seed heteromorphic annual plant in the central highlands of Mexico. Achenes (single‐seeded fruits) vary continuously within heads but are classified by shape and position as central, intermediate, or peripheral morphs and as having adhesive awns or not. Here we quantify shape as a principal component score contrasting log length and width of achenes. Heads and their variation among populations are described in terms of maximum, minimum, and range of shape scores; the number of achenes per head; quantitative indices of the abruptness of shape shift; where in the head the most abrupt change in shape occurs; and what achene shapes have awns. First and second principal components of these descriptors summarize 86% of among‐population variation in achene and head morphology and correlate strongly with percent central achenes per head (%C) and percent of achenes with awns (%A), respectively. Awns are associated with greater dispersibility and achene shape is correlated with speed of dormancy loss. We hypothesized that dispersal morphology would be associated with vegetation attributes indicative of population ephemerality and that dormancy morphology would be associated with precipitation patterns during the early germination season. Morphological distance matrices were calculated using Euclidean distances among populations in %A and %C. Geographic distances among populations were calculated, as were genetic distances based on isozyme frequencies from 29 bands of six enzymes. Vegetation was classified as open or closed and early spring (germination season) and summer precipitation means were determined for each site. Closed vegetation was assumed to provide only ephemeral habitats for H. pinnatum. Partial matrix correlations between morphology and environment controlled for geographic but not genetic distance among sites, since the latter was not significantly correlated with either morphology or geography. A significant relationship was found between %A and closed vegetation, lower spring, and higher summer precipitation. %C was only correlated with lower spring precipitation. Independence of isozyme and morphological traits is interpreted in terms of selection on the latter but not the former.

On the factors that promote the diversity of herbivorous insects and plants in tropical forests

Significance A central mission in ecology has been to explain differences in biodiversity across the world and across groups of organisms. This knowledge is not only fundamental as a scientific objective but also for practical issues of major concern to humankind. Plants and phytophagous insects comprise the highest macroscopic diversity on Earth, making it particularly important to know the mechanisms that allow their species to coexist. This study suggests that without insect specialization the maintenance of tropical plant diversity might not be possible. Also, without high divergence of defenses among plants, insect tropical diversity may not persist either. Some of the most fascinating and challenging questions in ecology are why biodiversity is highest in tropical forests and whether the factors involved are unique to these habitats. I did a worldwide test of the hypotheses that plant community divergence in antiherbivore traits results in higher insect herbivore diversity, and that predominant attack by specialized herbivores promotes plant richness. I found strong correlative support for both ideas. Butterfly diversity was greatest in regions where the community average species-pairwise dissimilarity in antiherbivore traits among plant species was highest. There was also a strong positive relationship between specialized (insect) vs. generalized (mammal) herbivores and plant richness. Regions where herbivory impact by mammals was higher than that of insects tended to have lower plant diversities. In contrast, regions in which insects are the main consumers, particularly in the Central and South American tropics, had the highest plant richness. Latitude did not explain any residual variance in insect or plant richness. The strong connections found between insect specialization, plant defense divergence, and plant and insect diversities suggest that increasing our understanding of the ecology of biological communities can aid in considerations of how to preserve biodiversity in the future.