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Asexual reproduction imposes evolutionary handicaps on asexual species, rendering them prone to extinction, because asexual reproduction generates novel genotypes and purges deleterious mutations at lower rates than sexual reproduction. Here, we report the first case of complete asexuality in ants, the fungus-growing ant Mycocepurus smithii, where queens reproduce asexually but workers are sterile, which is doubly enigmatic because the clonal colonies of M. smithii also depend on clonal fungi for food. Degenerate female mating anatomy, extensive field and laboratory surveys, and DNA fingerprinting implicate complete asexuality in this widespread ant species. Maternally inherited bacteria (e.g. Wolbachia, Cardinium) and the fungal cultivars can be ruled out as agents inducing asexuality. M. smithii societies of clonal females provide a unique system to test theories of parent-offspring conflict and reproductive policing in social insects. Asexuality of both ant farmer and fungal crop challenges traditional views proposing that sexual farmer ants outpace coevolving sexual crop pathogens, and thus compensate for vulnerabilities of their asexual crops. Either the double asexuality of both farmer and crop may permit the host to fully exploit advantages of asexuality for unknown reasons or frequent switching between crops (symbiont reassociation) generates novel ant-fungus combinations, which may compensate for any evolutionary handicaps of asexuality in M. smithii.

Fungus-growing ants (Attini) are part of a complex symbiosis with Basidiomycetous fungi, which the ants cultivate for food, Ascomycetous fungal pathogens (Escovopsis), which parasitize cultivars, and Actinobacteria, which produce antibiotic compounds that suppress pathogen growth. Earlier studies that have characterized the association between attine ants and their bacterial symbionts have employed broad phylogenetic approaches, with conclusions ranging from a diffuse coevolved mutualism to no specificity being reported. However, the geographic mosaic theory of coevolution proposes that coevolved interactions likely occur at a level above local populations but within species. Moreover, the scale of population subdivision is likely to impact coevolutionary dynamics. Here, we describe the population structure of bacteria associated with the attine Apterostigma dentigerum across Central America using multilocus sequence typing (MLST) of six housekeeping genes. The majority (90%) of bacteria that were isolated grouped into a single clade within the genus Pseudonocardia. In contrast to studies that have suggested that Pseudonocardia dispersal is high and therefore unconstrained by ant associations, we found highly structured () and dispersal-limited (i.e., significant isolation by distance; , ) populations over even a relatively small scale (e.g., within the Panama Canal Zone). Estimates of recombination versus mutation were uncharacteristically low compared with estimates for free-living Actinobacteria (e.g., in La Selva, Costa Rica), which suggests that recombination is constrained by association with ant hosts. Furthermore, Pseudonocardia population structure was correlated with that of Escovopsis species (, ), supporting the bacteria's role in disease suppression. Overall, the population dynamics of symbiotic Pseudonocardia are more consistent with a specialized mutualistic association than with recently proposed models of low specificity and frequent horizontal acquisition.

Taxonomic confusion and limited data have impeded species-level biogeographic analyses of the world’s largest bony fishes, ocean sunfishes (Molidae; ‘molids’), in many ecosystems. However, recent advances in molid taxonomy and the emergence of photo-based community-science platforms provide an opportunity to revisit species-level biogeography. In this study, we use crowd-sourced images of 1,213 ocean sunfishes to determine if molid morphology visible in citizen-science images permits reliable species determination. From the ensuing data, we describe patterns in molid size structure and species composition from 1,178 molids observed in the Alaska and California Current Systems (ACS and CCS, respectively). Molids <1 m total length (TL) were commonly reported in the CCS, particularly off the central coast of California, suggesting this area may function as a molid nursery. Molids >1 m TL were more commonly observed in both the CCS and cooler ACS, which suggests larger molids occupy a larger thermal range (ontogenetic habitat expansion) than smaller individuals. Overall, Mola mola was the most frequently observed species in both the ACS and CCS; however, the persistent occurrence of Mola tecta in both current systems suggests a range extension for this otherwise Southern Hemisphere species. The species identity of six M. tecta specimens from California and Alaska were verified with genetic analysis. Finally, two Mola alexandrini confirmed in the southern portion of the CCS represent the first records of this species in the Northeast Pacific Ocean.

The ecological and evolutionary dynamics of newly introduced invasive species can best be understood by identifying the source population(s) from which they originated, as many species vary behaviorally, morphologically, and genetically across their native landscapes. We attempt to identify the source(s) of the red imported fire ant ( Solenopsis invicta ) in the southern USA utilizing data from three classes of genetic markers (allozymes, microsatellites, and mitochondrial DNA sequences) and employing Bayesian clustering simulations, assignment and exclusion tests, and phylogenetic and population genetic analyses. We conclude that the Mesopotamia flood plain near Formosa, Argentina represents the most probable source region for introduced S. invicta among the 10 localities sampled across the native South American range. This result confirms previous suspicions that the source population resides in northern Argentina, while adding further doubts to earlier claims that the Pantanal region of Brazil is the source area. Several lines of evidence suggest that S. invicta in the southern USA is derived from a single location rather than being the product of multiple invasions from widely separated source localities. Although finer-scale sampling of northern Argentina and Paraguay combined with the use of additional genetic markers will be necessary to provide a highly precise source population assignment, our current results are of immediate use in directing future sampling and focusing ongoing biological control efforts.

The distribution of genetic and phenotypic variation in both hosts and parasites over their geographic ranges shapes coevolutionary dynamics. Specifically, concordant host and parasite distributions facilitate localized adaptation and further specialization of parasite genotypes on particular host genotypes. We here compare genetic population structure of the cultivated fungi of the fungus-growing ant Apterostigma dentigerum and of the cultivar-attacking fungus, Escovopsis, to determine whether these microbial associations have evolved or are likely to evolve genotype–genotype specialization. Analyses based on amplified fragment length polymorphism (AFLP) genotyping of host cultivars and pathogenic Escovopsis from 77 A. dentigerum colonies reveal that populations of hosts and pathogens are not similarly diverged and that host and pathogen genetic distances are uncorrelated, indicating that genetically similar parasites are not infecting genetically similar hosts. Microbial bioassays between pathogens and cultivars of different genotypes and from different populations show little pairwise specificity; most Escovopsis strains tested can successfully infect all cultivar strains with which they are paired. These molecular and experimental data suggest that Escovopsis genotypes are not tightly tracking cultivar genotypes within the A. dentigerum system. The diffuse nature of this host–pathogen association, in which pathogen genotypes are not interacting with a single host genotype but instead with many different hosts, will influence evolutionary and ecological disease dynamics of the fungus-growing ant–microbe symbiosis.

Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldiers, resulting in one of the most complex polymorphic caste systems within ants. To begin uncovering the genomic underpinnings of this system, we sequenced the genome of Atta cephalotes using 454 pyrosequencing. One prediction from this ant's lifestyle is that it has undergone genetic modifications that reflect its obligate dependence on the fungus for nutrients. Analysis of this genome sequence is consistent with this hypothesis, as we find evidence for reductions in genes related to nutrient acquisition. These include extensive reductions in serine proteases (which are likely unnecessary because proteolysis is not a primary mechanism used to process nutrients obtained from the fungus), a loss of genes involved in arginine biosynthesis (suggesting that this amino acid is obtained from the fungus), and the absence of a hexamerin (which sequesters amino acids during larval development in other insects). Following recent reports of genome sequences from other insects that engage in symbioses with beneficial microbes, the A. cephalotes genome provides new insights into the symbiotic lifestyle of this ant and advances our understanding of host-microbe symbioses.

Fungus-growing ants (Attini) are part of a complex symbiosis with Basidiomycetous fungi, which the ants cultivate for food, Ascomycetous fungal pathogens (Escovopsis), which parasitize cultivars, and Actinobacteria, which produce antibiotic compounds that suppress pathogen growth. Earlier studies that have characterized the association between attine ants and their bacterial symbionts have employed broad phylogenetic approaches, with conclusions ranging from a diffuse coevolved mutualism to no specificity being reported. However, the geographic mosaic theory of coevolution proposes that coevolved interactions likely occur at a level above local populations but within species. Moreover, the scale of population subdivision is likely to impact coevolutionary dynamics. Here, we describe the population structure of bacteria associated with the attineApterostigma dentigerumacross Central America using multilocus sequence typing (MLST) of six housekeeping genes. The majority (90%) of bacteria that were isolated grouped into a single clade within the genusPseudonocardia. In contrast to studies that have suggested thatPseudonocardiadispersal is high and therefore unconstrained by ant associations, we found highly structured ( ) and dispersal-limited (i.e., significant isolation by distance; , ) populations over even a relatively small scale (e.g., within the Panama Canal Zone). Estimates of recombination versus mutation were uncharacteristically low compared with estimates for free-living Actinobacteria (e.g., in La Selva, Costa Rica), which suggests that recombination is constrained by association with ant hosts. Furthermore,Pseudonocardiapopulation structure was correlated with that ofEscovopsisspecies ( , ), supporting the bacteria’s role in disease suppression. Overall, the population dynamics of symbioticPseudonocardiaare more consistent with a specialized mutualistic association than with recently proposed models of low specificity and frequent horizontal acquisition.

Microbial symbionts play key roles in shaping the diversity of life, from disease causing pathogens to beneficial microbes. The fungus-growing ant (Attini, Apterostigma dentigerum) is ideal for exploring these dynamics, as it maintains multiple symbionts, including fungal cultivars, cultivar attacking pathogens, and mutualistic bacteria whose antibiotic secretions combat infection. Decades of Attine-symbiont research has characterized these interactions as examples of diffuse coevolution. By contrast, coevolutionary theory on a geographic scale posits that these diffuse associations may still contain tightly coevolved interactions in a mosaic pattern over space. Moreover, these mosaics are shaped by the population genetic structure of interacting species. In this dissertation, I characterize the Apterostigma dentigerum -symbiont dynamic from a geographic mosaic prospective. The history of attine-symbiont evolutionary ecology is reviewed in chapter 1. In chapter 2, I describe cultivar-pathogen population structure and suggest that this labile association may facilitate specific adaptation by the mutualistic bacteria, Pseudonocardia. In chapter 3, I describe the population genetic structure of Pseudonocardia and demonstrate that its fine scale phylogeograpic structure may facilitate local adaptation with a common pathogen ( Escovopsis) morphotype. Chapter 4 uses bioassay inhibition experiments in combination with population genomic approaches to demonstrate that the Pseudonocardia-Escovopsis interaction is consistent with a geographic mosaic of coevolution, with a locally adapted population residing on Barro Colorado Island in Panama. Chapter 5 provides a putative framework and future directions for understanding the role biosynthetic gene clusters play in Pseudonocardia-pathogen coevolution. These studies provide insights into the maintenance of antibiotic potency over evolutionary time, and microbial niche evolution.

The distribution of genetic and phenotypic variation in both hosts and parasites over their geographic ranges shapes coevolutionary dynamics. Specifically, concordant host and parasite distributions facilitate localized adaptation and further specialization of parasite genotypes on particular host genotypes. We here compare genetic population structure of the cultivated fungi of the fungus-growing ant Apterostigma dentigerum and of the cultivar-attacking fungus, Escovopsis , to determine whether these microbial associations have evolved or are likely to evolve genotype–genotype specialization. Analyses based on amplified fragment length polymorphism (AFLP) genotyping of host cultivars and pathogenic Escovopsis from 77 A. dentigerum colonies reveal that populations of hosts and pathogens are not similarly diverged and that host and pathogen genetic distances are uncorrelated, indicating that genetically similar parasites are not infecting genetically similar hosts. Microbial bioassays between pathogens and cultivars of different genotypes and from different populations show little pairwise specificity; most Escovopsis strains tested can successfully infect all cultivar strains with which they are paired. These molecular and experimental data suggest that Escovopsis genotypes are not tightly tracking cultivar genotypes within the A. dentigerum system. The diffuse nature of this host–pathogen association, in which pathogen genotypes are not interacting with a single host genotype but instead with many different hosts, will influence evolutionary and ecological disease dynamics of the fungus-growing ant–microbe symbiosis.

The geographic and phylogenetic scale of ecologically relevant microbial diversity is still poorly understood. Using a model mutualism, fungus-growing ants and their defensive bacterial associate Pseudonocardia, we analyzed genetic diversity and biosynthetic potential in 46 strains isolated from ant colonies in a 20km transect near Barro Colorado Island in Panama. Despite an average pairwise core genome similarity of greater than 99%, population genomic analysis revealed several distinct bacterial populations matching ant host geographic distribution. We identified both genetic diversity signatures and divergent genes distinct to each lineage. We also identify natural product biosynthesis clusters specific to isolation locations. These geographic patterns were observable despite the populations living in close proximity to each other and provides evidence of ongoing genetic exchange. Our results add to the growing body of literature suggesting that variation in traits of interest can be found at extremely fine phylogenetic scales.