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Myriad Mirids: The spectacular radiation of Pseudoloxops (Hemiptera: Miridae) plant bugs in French Polynesia (and the kids that love them!)

  • Author(s): Balukjian, Bradley James
  • Advisor(s): Gillespie, Rosemary G
  • et al.
Abstract

Studies of natural history and biodiversity may not top most funding agencies' priority lists, but they should. It is an exciting time for the field of biology--we are sequencing whole genomes, devising sophisticated models to cope with accelerating climate change, and even tinkering with the possibility of bringing extinct species back to life. But in the meantime, we continue to ignore the documentation and discovery of the vast majority of extant life on our planet. Millions of species, each with their own unique evolutionary history and trajectory, remain unknown, waiting to tell us their story and teach us their strategies for success. Here, my collaborators and I demonstrate the importance of documenting the diversity contained within a single lineage of insects, from examining the best methods for accurately determining numbers of species to showing the downstream benefits of incorporating that knowledge into local education for the benefit of all.

In the first chapter, we revise the taxonomy of a lineage of plant bugs (Hemiptera: Miridae) that has radiated in the islands of French Polynesia. Six species of endemic Pseudoloxops/italic> plant bugs were previously known from two islands in French Polynesia, indicating a small radiation. We collected ecological, morphological, molecular, and geographical data for hundreds of fresh and historical Pseudoloxops/italic> specimens, expanding the genus' range to nine islands in two archipelagoes (the Austral and Society Islands). We combined all of the above data sources in an iterative integrative taxonomy framework to test the six existing species hypotheses and to search for new diversity. We confirmed 3 of the 6 original species designations and synonymized the remaining 3 species, and delimited and described an additional 23 species, for a total of 26. Our analysis demonstrates the value of an integrative approach, as we discovered cryptic species and color polymorphism that may have been missed or misinterpreted using a species concept that relied on a single line of evidence. We also found evidence for population-level diversification and discuss the potential for future research on the role of color in this radiation.

In the second chapter, we explore the relative importance of ecology and geographic isolation in this lineage to provide a first approximation of whether the radiation was adaptive or non-adaptive. We collected Pseudoloxops/italic> from a wide range of plants, with 27 species in 25 different plant families and 13 orders. We then inferred a combined Bayesian molecular phylogeny from three genes, including 25 of the 26 known Pseudoloxops/italic> species, to examine the roles of plant affiliation and geography (island distribution) in speciation. We reconstructed the ancestral states using parsimony for these two characters, and found 12 speciation events that were well-supported in the phylogeny. Both plant-switching and island-hopping were correlated with speciation. For the 7 speciation events for which we could unequivocally determine plant affiliation before and after speciation, 4 were associated with a plant shift. For the 8 speciation events where island distribution could be reconstructed, two involved shifts to a new island. There were 5 cases for which we could determine both character states before and after speciation. In three of them, speciation occurred within the same locality with a switch in plant taxonomic order, suggesting that the lineage has great dietary versatility. However, much more research into feeding needs to be conducted, as anecdotal evidence from Pseudoloxops/italic> outside of French Polynesia suggests they may be facultative predators. In the other two speciation events, there was neither a geographic shift nor a change in plant affiliation, suggesting some other mechanism for speciation. Based on our results, both plant-switching and geography have played a role in the diversification of this radiation. Finally, plant switching from flowering plants (angiosperms) to ferns was observed in two different parts of the radiation. This finding was surprising for two reasons--first, plant bugs are rarely associated with ferns, likely because of their highly toxic secondary compounds, and second because the expectation on islands is that organisms colonize ferns first and then switch on to other plants, since ferns are often among the first plants to arrive on newly formed oceanic islands. While a better-resolved phylogeny is needed to reconstruct the timing of speciation events, the character polarity in our phylogeny indicates that angiosperm use is basal to fern use.

In the third chapter, we address the larger societal impact of taxonomic and biodiversity research by examining the effect of a natural history-driven curriculum on elementary schoolchildren's scientific knowledge. While studies have demonstrated the potential for natural history education to improve children's attitudes towards and knowledge of science and nature, few studies have been done in areas where indigenous culture heavily influences children's worldview. The lead author taught a nine-month natural history/biodiversity class focused on insects and plants to fifth-graders at the Pao Pao elementary school on the French Polynesian island of Moorea and tested their scientific knowledge before and after receiving the program. We compared their results to a control that did not receive the program, and while both cohorts improved, the experimental group's improvement was significantly greater (mean of 82.2% vs. 30.5%). We performed a delayed post-test evaluation three years after the conclusion of the program with a subset of the experimental cohort to test their retention and interest in science. A one-way ANOVA revealed significant differences between their pre-, post-, and delayed post-test scores, with the post- and follow-up scores significantly higher than the pre-scores. While the raw delayed post-test scores were lower than the post-scores, suggesting some regression, this finding was not statistically significant. The follow-up students also reported a strong interest in science, with 66.7% answering the question "Do you like science?" with "yes" and 20% with "sort of." They also indicated a strong affinity for insects and plants, with 50% of them volunteering insects as their favorite subject in science and 26.7% volunteering plants. Finally, the qualitative coding of the experimental group's test and survey responses revealed both the influence of indigenous culture on their scientific understanding and the appeal of taxonomy and field trips to children. When prompted for an example of a native plant, 24% of the experimental group named a plant introduced by the Polynesians, suggesting the misconception that plants with a prevalent role in indigenous culture have always been there. In the follow-up survey, 36.7% mentioned the field trips among their memories of the course, and 20% gave full scientific names for species they recalled from the class. The latter contrasts with the commonly held belief that taxonomy is too arcane to connect with the general public.

Overall, our research demonstrates the scientific and societal benefits of thorough natural history and biodiversity studies. The use of integrative methods allowed for the discovery of a staggering number of plant bug species in a very small area of land, and the documentation of ecological attributes allowed us to show how this radiation of bugs has been both adaptive and non-adaptive. The integration of this biodiversity information and a focus on traditionally "uncharismatic" groups of organisms (insects and plants) in local education provided substantial gains in schoolchildren's scientific knowledge, and perhaps more importantly, helped to popularize science and nature. Our hope is that this work inspires future graduate students to pursue research on the unknown and the undiscovered, and to link their findings directly to local communities.

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