Advances in the Evolution and Ecology of 13- and 17-Year Periodical Cicadas

Apart from model organisms, 13- and 17-year periodical cicadas (Hemiptera: Cicadidae: Magicicada) are among the most studied insects in evolution and ecology. They are attractive subjects because they predictably emerge in large numbers; have a complex biogeography shaped by both spatial and temporal isolation; and include three largely sympatric, parallel species groups that are, in a sense, evolutionary replicates. Magicicada are also relatively easy to capture and manipulate, and their spectacular, synchronized mass emergences facilitate outreach and citizen science opportunities. Since the last major review, studies of Magicicada have revealed insights into reproductive character displacement and the nature of species boundaries, provided additional examples of allochronic speciation, found evidence for repeated and parallel (but noncontemporaneous) evolution of 13- and 17-year life cycles, quantified the amount and direction of gene flow through time, revealed phylogeographic patterning resulting from paleoclimate change, studied the timing of juvenile development, and created hypotheses for the evolution of life-cycle control and the future effects of climate change on Magicicada life cycles. New ecological studies have supported and questioned the role of prime numbers in Magicicada ecology and evolution, found bidirectional shifts in population size over generations, quantified the contribution of Magicicada to nutrient flow in forest ecosystems, and examined behavioral and biochemical interactions between Magicicada and their fungal parasites and bacterial endosymbionts. Expected final online publication date for the Annual Review of Entomology, Volume 67 is January 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

How does the magnitude of genetic variation affect eco-evolutionary dynamics in character displacement?

While previous studies on character displacement tended to focus on trait divergence and convergence as a result of long-term evolution, recent studies suggest that character displacement can be a special case of evolutionary rescue, where rapid evolution prevents population extinction by weakening negative interspecific interactions. When the magnitude of genetic variation is small, however, the speed of trait divergence can be slow and populations may go extinct before the completion of character displacement. Here we analyzed a simple model to examine how the magnitude of genetic variation affects evolutionary rescue via ecological and reproductive character displacement that weakens resource competition and reproductive interference, respectively. We found that the large additive genetic variance is more important for preventing extinction in reproductive character displacement than in ecological character displacement. This is because reproductive interference produces a locally stable coexistence equilibrium with positive frequency-dependence (i.e., minority disadvantage) whereas ecological character displacement results in a globally stable coexistence equilibrium. Furthermore, population extinction becomes less likely when ecological and reproductive character displacement occur simultaneously due to positive covariance between ecological and reproductive traits. Our results suggest that while reproductive character displacement may be rarer than ecological character displacement, it is more likely to occur when there exists positive trait covariance, such as the case of a magic trait in reinforcement of speciation processes.

Asymmetric acoustic signal recognition led to asymmetric gene flow between two parapatric frogs

Correct discrimination between courtship signals could help to maintain genetic integrity between closely related species. However, asymmetric usage of signals might cause asymmetric gene flow across the contact zone. Buergeria choui and B. otai are sibling-species with a parapatric distribution pattern in Taiwan, having two narrow contact zones on the east and west sides of the island. Combining behavioural experiments with genome-wide RAD-seq analyses, we test whether the ability of signal recognition influences genetic introgression across their species boundary. The playback experiments show that all B. choui populations respond strongest to their own ‘cricket’ trills, while the western population of B. otai have evolved a strong level of reproductive character displacement by showing the inclusive usage of the unique ‘chicken’ signals. In contrast, the eastern B. otai population uses both ‘chicken’ and ‘cricket’ trills, and has a stronger preference for the latter. The weak reproductive character displacement in the eastern population has led to asymmetry genetic introgression from B. choui toward B. otai. Our results support the prediction that a more specialized signal-user, compared to its sibling, generalized signal-user, might have a higher probability of maintaining their genetic integrity in the secondary contact region.

Cryptic Diversity and Sexual Selection

Recent advances in molecular and genetic techniques have revealed tremendous hidden genetic diversity in plants and animals. Crustaceans are no exception and, in fact, present one of the highest levels of cryptic diversity among the metazoans. Beyond the importance of such discovery and its multiple implications for taxonomy and ecology, it is now timely to investigate the potential causes of cryptic diversity. This chapter reviews the theoretical and experimental literature, seeking evidences for a relationship between sexual selection and cryptic diversity in crustaceans. It proposes three scenarios for the role of sexual selection on the origin and maintenance of pre-mating isolation and genetic divergence among crustacean populations, and suggests ways to discriminate among them experimentally or using existing data. Assuming that taxonomic identification is largely based on differences in sexually selected morphological traits, it also reviews evidence for a cryptic action of sexual selection on crustacean phenotypes. Specifically, if sexual selection acts primarily on chemical, visual, or behavioral traits, it is likely that allopatric crustacean populations remain morphologically similar even when they are reproductively isolated. This review shows that the strength of sexual selection likely differs among allopatric populations but does not seem to consistently induce pre-mating isolation (e.g. as in copepods and amphipods). Research is now needed to try to identify general patterns and determine the role of sexual selection on pre-mating isolation after secondary contact between populations, through reinforcement and reproductive character displacement.

Phenological displacement is uncommon among sympatric angiosperms

Interactions between species can influence access to resources and successful reproduction. One possible outcome of such interactions is reproductive character displacement. Here, the similarity of reproductive traits – such as flowering time – among close relatives growing in sympatry differ more so than when growing apart. However, evidence for the overall prevalence and direction of this phenomenon, or the stability of such differences under environmental change, remains untested across large taxonomic and spatial scales. We apply data from tens of thousands of herbarium specimens to examine character displacement in flowering time across 110 animal-pollinated angiosperm species in the eastern USA. We demonstrate that the degree and direction of phenological displacement among co-occurring closely related species pairs varies tremendously. Overall, flowering time displacement in sympatry is not common. However, displacement is generally greater among species pairs that flower close in time, regardless of direction. We additionally identify that future climate change may alter the nature of phenological displacement among many of these species pairs. On average, flowering times of closely related species were predicted to shift further apart by the mid-21st century, which may have significant future consequences for species interactions and gene flow.