Evolution of Mimicry Rings as a Window into Community Dynamics

Mimicry rings are communities of mimetic organisms that are excellent models for ecological and evolutionary studies because the community composition, the nature of the species interactions, the phenotypes under selection, and the selective agents are well characterized. Here, we review how regional and ecological filtering, density- and frequency-dependent selection, toxicity of prey, and age of mimicry rings shape their assembly. We synthesize findings from theoretical and empirical studies to generate the following hypotheses: ( a) the degree of unpalatability and age of mimicry rings increase mimicry ring size and ( b) the degree of unpalatability, generalization of the aposematic signal, and availability of alternative prey are positively related to the breadth of the protection umbrella for an aposematic signal and negatively related to the degree of mimetic resemblance. We also provide a phylogenetic framework in which key aspects of mimicry ring diversification may be studied. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 52 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Rethinking the Plant Economics Spectrum for Annuals: A Multi-Species Study

The plant economics spectrum hypothesizes a correlation among resource-use related traits along one single axis, which determines species’ growth rates and their ecological filtering along resource gradients. This concept has been mostly investigated and shown in perennial species, but has rarely been tested in annual species. Annuals evade unfavorable seasons as seeds and thus may underlie different constraints, with consequences for interspecific trait-trait, trait-growth, and trait-environment relations. To test the hypotheses of the plant economics spectrum in annual species, we measured twelve resource-use related leaf and root traits in 30 winter annuals from Israel under controlled conditions. Traits and their coordinations were related to species’ growth rates (for 19 species) and their distribution along a steep rainfall gradient. Contrary to the hypotheses of the plant economics spectrum, in the investigated annuals traits were correlated along two independent axes, one of structural traits and one of carbon gain traits. Consequently, species’ growth rates were related to carbon gain traits, but independent from structural traits. Species’ distribution along the rainfall gradient was unexpectedly neither associated with species’ scores along the axes of carbon gain or structural traits nor with growth rate. Nevertheless, root traits were related with species’ distribution, indicating that they are relevant for species’ filtering along rainfall gradients in winter annuals. Overall, our results showed that the functional constraints hypothesized by the plant economics spectrum do not apply to winter annuals, leading to unexpected trait-growth and trait-rainfall relations. Our study thus cautions to generalize trait-based concepts and findings between life-history strategies. To predict responses to global change, trait-based concepts should be explicitly tested for different species groups.

Assembly and seasonality of core phyllosphere microbiota on perennial biofuel crops

Perennial grasses are promising feedstocks for biofuel production, with potential for leveraging their native microbiomes to increase their productivity and resilience to environmental stress. Here, we characterize the 16S rRNA gene diversity and seasonal assembly of bacterial and archaeal microbiomes of two perennial cellulosic feedstocks, switchgrass (Panicum virgatum L.) and miscanthus (Miscanthus x giganteus). We sample leaves and soil every three weeks from pre-emergence through senescence for two consecutive switchgrass growing seasons and one miscanthus season, and identify core leaf taxa based on occupancy. Virtually all leaf taxa are also detected in soil; source-sink modeling shows non-random, ecological filtering by the leaf, suggesting that soil is an important reservoir of phyllosphere diversity. Core leaf taxa include early, mid, and late season groups that were consistent across years and crops. This consistency in leaf microbiome dynamics and core members is promising for microbiome manipulation or management to support crop production.

Many Options, Few Solutions: Over 60 My Snakes Converged on a Few Optimal Venom Formulations

Gene expression changes contribute to complex trait variations in both individuals and populations. However, the evolution of gene expression underlying complex traits over macroevolutionary timescales remains poorly understood. Snake venoms are proteinaceous cocktails where the expression of each toxin can be quantified and mapped to a distinct genomic locus and traced for millions of years. Using a phylogenetic generalized linear mixed model, we analyzed expression data of toxin genes from 52 snake species spanning the 3 venomous snake families and estimated phylogenetic covariance, which acts as a measure of evolutionary constraint. We find that evolution of toxin combinations is not constrained. However, although all combinations are in principle possible, the actual dimensionality of phylomorphic space is low, with envenomation strategies focused around only four major toxin families: metalloproteases, three-finger toxins, serine proteases, and phospholipases A2. Although most extant snakes prioritize either a single or a combination of major toxin families, they are repeatedly recruited and lost. We find that over macroevolutionary timescales, the venom phenotypes were not shaped by phylogenetic constraints, which include important microevolutionary constraints such as epistasis and pleiotropy, but more likely by ecological filtering that permits a small number of optimal solutions. As a result, phenotypic optima were repeatedly attained by distantly related species. These results indicate that venoms evolve by selection on biochemistry of prey envenomation, which permit diversity through parallelism, and impose strong limits, since only a few of the theoretically possible strategies seem to work well and are observed in extant snakes.

Many options, few solutions: over 60 million years snakes converged on a few optimal venom formulations

Gene expression changes contribute to complex trait variations in both individuals and populations. However, how gene expression influences changes of complex traits over macroevolutionary timescales remains poorly understood. Being comprised of proteinaceous cocktails, snake venoms are unique in that the expression of each toxin can be quantified and mapped to a distinct genomic locus and traced for millions of years. Using a phylogenetic generalized linear mixed model, we analysed expression data of toxin genes from 52 snake species spanning the three venomous snake families, and estimated phylogenetic covariance, which acts as a measure of evolutionary constraint. We find that evolution of toxin combinations is not constrained. However, while all combinations are in principle possible, the actual dimensionality of phylomorphic space is low, with envenomation strategies focused around only four major toxins: metalloproteases, three-finger toxins, serine proteases, and phospholipases A2. While most extant snakes prioritize either a single or a combination of major toxins, they are repeatedly recruited and lost. We find that over macroevolutionary timescales the venom phenotypes were not shaped by phylogenetic constraints, which include important microevolutionary constraints such as epistasis and pleiotropy, but more likely by ecological filtering that permits a few optimal solutions. As a result, phenotypic optima were repeatedly attained by distantly related species. These results indicate that venoms evolve by selection on biochemistry of prey envenomation, which permit diversity though parallelism and impose strong limits, since only a few of the theoretically possible strategies seem to work well and are observed in extant snakes.