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"Goldman, Benjamin"
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Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet
by
Lapoint, Richard T.
,
Hildebrand, John G.
,
Faucher, Cécile P.
in
ancestry
,
Animals
,
Biological Sciences
2015
Significance The evolution of herbivory in animals is rare but has resulted in major adaptive radiations. Its rarity suggests that there are barriers to colonization of plants. Behavioral adaptations, involving host plant finding, are likely the first to evolve during the transition to herbivory. A recently evolved herbivorous fly species was derived from yeast-feeding ancestors. This herbivorous fly, unlike its yeast-feeding relatives, lost attraction to yeast volatiles, the ability to detect yeast volatiles, and three genes that encode olfactory receptors critical for detecting yeast volatiles in Drosophila melanogaster . Loss-of-function mutations may play a role in the transition to herbivory in insects, which account for nearly 25% of all species of life.
Herbivory is a key innovation in insects, yet has only evolved in one-third of living orders. The evolution of herbivory likely involves major behavioral changes mediated by remodeling of canonical chemosensory modules. Herbivorous flies in the genus Scaptomyza (Drosophilidae) are compelling species in which to study the genomic architecture linked to the transition to herbivory because they recently evolved from microbe-feeding ancestors and are closely related to Drosophila melanogaster . We found that Scaptomyza flava , a leaf-mining specialist on plants in the family (Brassicaceae), was not attracted to yeast volatiles in a four-field olfactometer assay, whereas D. melanogaster was strongly attracted to these volatiles. Yeast-associated volatiles, especially short-chain aliphatic esters, elicited strong antennal responses in D. melanogaster , but weak antennal responses in electroantennographic recordings from S. flava . We sequenced the genome of S. flava and characterized this species’ odorant receptor repertoire. Orthologs of odorant receptors, which detect yeast volatiles in D. melanogaster and mediate critical host-choice behavior, were deleted or pseudogenized in the genome of S. flava . These genes were lost step-wise during the evolution of Scaptomyza . Additionally, Scaptomyza has experienced gene duplication and likely positive selection in paralogs of Or67b in D. melanogaster . Olfactory sensory neurons expressing Or67b are sensitive to green-leaf volatiles. Major trophic shifts in insects are associated with chemoreceptor gene loss as recently evolved ecologies shape sensory repertoires.
Journal Article
Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants
2009
Ants are a dominant feature of terrestrial ecosystems, yet we know little about the forces that drive their evolution. Recent findings illustrate that their diets range from herbivorous to predaceous, with \"herbivores\" feeding primarily on exudates from plants and sap-feeding insects. Persistence on these nitrogen-poor food sources raises the question of how ants obtain sufficient nutrition. To investigate the potential role of symbiotic microbes, we have surveyed 283 species from 18 of the 21 ant subfamilies using molecular techniques. Our findings uncovered a wealth of bacteria from across the ants. Notable among the surveyed hosts were herbivorous \"turtle ants\" from the related genera Cephalotes and Procryptocerus (tribe Cephalotini). These commonly harbored bacteria from ant-specific clades within the Burkholderiales, Pseudomonadales, Rhizobiales, Verrucomicrobiales, and Xanthomonadales, and studies of lab-reared Cephalotes varians characterized these microbes as symbiotic residents of ant guts. Although most of these symbionts were confined to turtle ants, bacteria from an ant-specific clade of Rhizobiales were more broadly distributed. Statistical analyses revealed a strong relationship between herbivory and the prevalence of Rhizobiales gut symbionts within ant genera. Furthermore, a consideration of the ant phylogeny identified at least five independent origins of symbioses between herbivorous ants and related RHIZOBIALES: Combined with previous findings and the potential for symbiotic nitrogen fixation, our results strongly support the hypothesis that bacteria have facilitated convergent evolution of herbivory across the ants, further implicating symbiosis as a major force in ant evolution.
Journal Article
Evolution of Olfactory Receptors Tuned to Mustard Oils in Herbivorous Drosophilidae
by
Verster, Kirsten I
,
Ramírez, Santiago R
,
Reisenman, Carolina E
in
Animals
,
Attractants
,
Biocompatibility
2022
Abstract
The diversity of herbivorous insects is attributed to their propensity to specialize on toxic plants. In an evolutionary twist, toxins betray the identity of their bearers when herbivores coopt them as cues for host-plant finding, but the evolutionary mechanisms underlying this phenomenon are poorly understood. We focused on Scaptomyza flava, an herbivorous drosophilid specialized on isothiocyanate (ITC)-producing (Brassicales) plants, and identified Or67b paralogs that were triplicated as mustard-specific herbivory evolved. Using in vivo heterologous systems for the expression of olfactory receptors, we found that S. flava Or67bs, but not the homologs from microbe-feeding relatives, responded selectively to ITCs, each paralog detecting different ITC subsets. Consistent with this, S. flava was attracted to ITCs, as was Drosophila melanogaster expressing S. flava Or67b3 in the homologous Or67b olfactory circuit. ITCs were likely coopted as olfactory attractants through gene duplication and functional specialization (neofunctionalization and subfunctionalization) in S. flava, a recently derived herbivore.
Journal Article
Asynchronous Diversification in a Specialized Plant-Pollinator Mutualism
by
Fujiwara, Mikiko K.
,
Eltz, Thomas
,
Pierce, Naomi E.
in
Angiosperms
,
Animal and plant ecology
,
Animal, plant and microbial ecology
2011
Most flowering plants establish mutualistic associations with insect pollinators to facilitate sexual reproduction. However, the evolutionary processes that gave rise to these associations remain poorly understood. We reconstructed the times of divergence, diversification patterns, and interaction networks of a diverse group of specialized orchids and their bee pollinators. In contrast to a scenario of coevolution by race formation, we show that fragrance-producing orchids originated at least three times independently after their fragrance-collecting bee mutualists. Whereas orchid diversification has apparently tracked the diversification of orchids' bee pollinators, bees appear to have depended on the diverse chemical environment of neotropical forests. We corroborated this apparent asymmetrical dependency by simulating co-extinction cascades in real interaction networks that lacked reciprocal specialization. These results suggest that the diversification of insect-pollinated angiosperms may have been facilitated by the exploitation of preexisting sensory biases of insect pollinators.
Journal Article
A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review
2012
Maternally transmitted bacteria have been important players in the evolution of insects and other arthropods, affecting their nutrition, defense, development, and reproduction. Wolbachia are the best studied among these and typically the most prevalent. While several other bacteria have independently evolved a heritable lifestyle, less is known about their host ranges. Moreover, most groups of insects have not had their heritable microflora systematically surveyed across a broad range of their taxonomic diversity. To help remedy these shortcomings we used diagnostic PCR to screen for five groups of heritable symbionts-Arsenophonus spp., Cardinium hertigii, Hamiltonella defensa, Spiroplasma spp., and Wolbachia spp.-across the ants and lepidopterans (focusing, in the latter case, on two butterfly families-the Lycaenidae and Nymphalidae). We did not detect Cardinium or Hamiltonella in any host. Wolbachia were the most widespread, while Spiroplasma (ants and lepidopterans) and Arsenophonus (ants only) were present at low levels. Co-infections with different Wolbachia strains appeared especially common in ants and less so in lepidopterans. While no additional facultative heritable symbionts were found among ants using universal bacterial primers, microbes related to heritable enteric bacteria were detected in several hosts. In summary, our findings show that Wolbachia are the dominant heritable symbionts of ants and at least some lepidopterans. However, a systematic review of symbiont frequencies across host taxa revealed that this is not always the case across other arthropods. Furthermore, comparisons of symbiont frequencies revealed that the prevalence of Wolbachia and other heritable symbionts varies substantially across lower-level arthropod taxa. We discuss the correlates, potential causes, and implications of these patterns, providing hypotheses on host attributes that may shape the distributions of these influential bacteria.
Journal Article
Specialization and Geographic Isolation Among Wolbachia Symbionts from Ants and Lycaenid Butterflies
by
Stahlhut, Julie K.
,
Moreau, Corrie S.
,
Pierce, Naomi E.
in
Animals
,
Ants
,
Ants - microbiology
2009
Wolbachia are the most prevalent and influential bacteria described among the insects to date. But despite their significance, we lack an understanding of their evolutionary histories. To describe the evolution of symbioses between Wolbachia and their hosts, we surveyed global collections of two diverse families of insects, the ants and lycaenid butterflies. In total, 54 Wolbachia isolates were typed using a Multi Locus Sequence Typing (MLST) approach, in which five unlinked loci were sequenced and analyzed to decipher evolutionary patterns. AMOVA and phylogenetic analyses demonstrated that related Wolbachia commonly infect related hosts, revealing a pattern of host association that was strongest among strains from the ants. A review of the literature indicated that horizontal transfer is most successful when Wolbachia move between related hosts, suggesting that patterns of host association are driven by specialization on a common physiological background. Aside from providing the broadest and strongest evidence to date for Wolbachia specialization, our findings also reveal that strains from New World ants differ markedly from those in ants from other locations. We, therefore, conclude that both geographic and phylogenetic barriers have promoted evolutionary divergence among these influential symbionts.
Journal Article
Essays in Labor and Public Economics
2024
In the first essay, we study why Americans rarely marry outside of their race or class group. We distinguish between two possible explanations: a lack of exposure to other groups versus a preference to marry within group. We develop an instrument for neighborhood exposure to opposite-sex members of other race and class groups using variation in sex ratios among nearby birth cohorts in childhood neighborhoods. We then test whether increased exposure results in more interracial (white-Black) and interclass (top-to-bottom parent income quartile) marriages. Increased exposure to opposite-sex members of other class groups generates a substantial increase in interclass marriage, but increased exposure to other race groups has no detectable effect on interracial marriage. We use these results to estimate a spatial model of the marriage market and quantify the impact of reducing residential segregation in general equilibrium. For small changes in exposure, the model implies effects in line with recent estimates from policy experiments. We then use the model to assess the overall contribution of segregation and find that residential segregation has large effects on interclass, but not interracial, marriage. In the second essay, we analyze the adult earnings impacts of the largest comprehensive student support program in the United States. Communities in Schools (CIS) places a “navigator” in high-poverty schools who provides an integrated system of supports to students, including academic (e.g., tutoring), economic (e.g., access to food assistance, housing), and mentoring. In 2023, CIS worked with 1.8 million students in 3,750 schools. Using later-treated CIS schools as a control, we estimate that four years of exposure to CIS generates a $1,500 (6% of control mean) increase in earnings at age 30. Effects are larger for students from low-income families and are driven by a reduction in non-employment and an increase in the probability of having a low-paying job. Each child exposed to four years of CIS is expected to pay an additional $9,000 in taxes between ages 18-65, which compares favorably to the direct cost of the program. Our results are relevant for the growing community school movement and illuminate a possible path for improving economic mobility in low opportunity neighborhoods. In the third essay, we use worker-level data on industry, occupation, and place of work to explore differences in the spatial properties of production, administrative, and R&D occupation groups within industries. To measure differences, we calculate location quotients at the local labor market level and the Duranton and Overman (2005) agglomeration index for each group. We find appreciable differences in the spatial distribution of occupation groups within most manufacturing industries, with R&D occupations consistently exhibiting the highest degree of spatial concentration. Our results are consistent with the core theoretical and empirical results in the agglomeration literature.
Dissertation