Influence of host phylogeny, geographical location and seed harvesting diet on the bacterial community of globally distributed Pheidole ants.
ABSTRACT: The presence of symbiotic relationships between organisms is a common phenomenon found across the tree of life. In particular, the association of bacterial symbionts with ants is an active area of study. This close relationship between ants and microbes can significantly impact host biology and is also considered one of the driving forces in ant evolution and diversification. Diet flexibility of ants may explain the evolutionary success of the group, which may be achieved by the presence of endosymbionts that aid in nutrition acquisition from a variety of food sources. With more than 1,140 species, ants from the genus Pheidole have a worldwide distribution and an important role in harvesting seeds; this behavior is believed to be a possible key innovation leading to the diversification of this group. This is the first study to investigate the bacterial community associated with Pheidole using next generation sequencing (NGS) to explore the influences of host phylogeny, geographic location and food preference in shaping the microbial community. In addition, we explore if there are any microbiota signatures related to granivory. We identified Proteobacteria and Firmicutes as the major phyla associated with these ants. The core microbiome in Pheidole (those found in >50% of all samples) was composed of 14 ASVs and the most prevalent are family Burkholderiaceae and the genera Acinetobacter, Streptococcus, Staphylococcus, Cloacibacterium and Ralstonia. We found that geographical location and food resource may influence the bacterial community of Pheidole ants. These results demonstrate that Pheidole has a relatively stable microbiota across species, which suggests the bacterial community may serve a generalized function in this group.
Project description:The objective of this study is to provide a detailed taxonomic resource for identifying and studying ants in the genus Pheidole that have established beyond their native ranges. There is an increasing need for systematists to study taxa of specific concern to 21(st) century environmental, food security and public health challenges. Systematics has an important role to play in both the theoretical and applied disciplines of invasion biology. Few invaders impact terrestrial ecosystems more than ants. Among the world's 100 worst invasive species is the cosmopolitan and highly destructive Pheidole megacephala (Fabricius). Accurate identification of Pheidole megacephala is imperative for the success of screening, management and eradication programs designed to protect native ecosystems from the impacts of this destructive species. However, accurate identification of Pheidole species is difficult because of their taxonomic diversity, dimorphic worker caste and lack of taxonomic resources. Illustrated keys are included, along with the taxonomic history, taxonomic diagnoses, biological notes and risk statements for the 14 most invasive members of the genus. Global distribution maps based on over 14,000 specimen and literature records are presented for each species. These results of this work will facilitate identification of pest species, determination of climatic and habitat requirements, discovery of pest origins, horizon scanning and assessment of invasion pathways. The following new synonym is proposed, with the senior synonym listed first and the junior synonyms in parentheses: Pheidole indica Mayr (= Pheidole teneriffana Forel, and its synonyms Pheidole taina Aguayo and Pheidole voeltzkowii Forel). Pheidole navigans Forel, stat. rev., stat. n. is removed from synonymy and elevated to species rank. It is proposed that records of Pheidole moerens Forel outside of the Mesoamerica and the Caribbean refer instead to Pheidole navigans or other heterospecific taxa in the Pheidole flavens species complex. We propose that the names Pheidole anastasii Emery and Pheidole floridana Emery have been widely misapplied to North American outdoor records of Pheidole bilimeki Mayr. It is suggested that the synonymy of Pheidole lauta Wheeler be transferred from Pheidole floridana Emery to Pheidole bilimeki Mayr.
Project description:The efficient investment of resources is often the route to ecological success, and the adaptability of resource investment may play a critical role in promoting biodiversity. The ants of the "hyperdiverse" genus Pheidole produce two discrete sterile castes, soldiers and minor workers. Within Pheidole, there is tremendous interspecific variation in proportion of soldiers. The causes and correlates of caste ratio variation among species of Pheidole remain enigmatic. Here we test whether a body size threshold model accounts for interspecific variation in caste ratio in Pheidole, such that species with larger body sizes produce relatively fewer soldiers within their colonies. We evaluated the caste ratio of 26 species of Pheidole and found that the body size of workers accounts for interspecific variation in the production of soldiers as we predicted. Twelve species sampled from one forest in Costa Rica yielded the same relationship as found in previously published data from many localities. We conclude that production of soldiers in the most species-rich group of ants is regulated by a body size threshold mechanism, and that the great variation in body size and caste ratio in Pheidole plays a role in niche divergence in this rapidly evolving taxon.
Project description:The ant genus Pheidole-for all of its hyperdiversity and global ubiquity-is remarkably conservative with regard to morphological disparity. A striking exception to this constrained morphology is the spinescent morphotype, which has evolved multiple times across distantly related lineages of Indoaustralian Pheidole. The Pheidole cervicornis group contains perhaps the most extraordinary spinescent forms of all Pheidole. Here we present a taxonomic revision of the P. cervicornis group, and use microtomographic scanning technology to investigate the internal anatomy of the thoracic spines. Our findings suggest the pronotal spines of Pheidole majors, are possibly skeletomuscular adaptations for supporting their disproportionately large heads. The 'head support hypothesis' is an alternative to the mechanical defense hypothesis most often used to explain spinescence in ants. The P. cervicornis group is known only from New Guinea and is represented by the following four species, including two described here as new: P. barumtaun Donisthorpe, P. drogon sp. nov., P. cervicornis Emery, and P. viserion sp. nov. The group is most readily identified by the minor worker caste, which has extremely long pronotal spines and strongly bifurcating propodeal spines. The major and minor workers of all species are illustrated with specimen photographs, with the exception of the major worker of P. cervicornis, which is not known.
Project description:The Fijian islands, a remote archipelago in the southwestern Pacific, are home to a number of spectacular endemic radiations of plants and animals. Unlike most Pacific archipelagos, these evolutionary radiations extend to social insects, including ants. One of the most dramatic examples of ant radiation in Fiji has occurred in the hyperdiverse genus Pheidole. Most of the 17 native Fijian Pheidole belong to one of two species groups that descended from a single colonization, yet have evolved dramatically contrasting morphologies: the spinescent P. roosevelti species group, and the more morphologically conservative P. knowlesi species group. Here we revise the knowlesi group, in light of recent phylogenetic results, and enhanced with modern methods of X-ray microtomography. We recognize six species belonging to this group, including two of which we describe as new: Pheidole caldwelli Mann, Pheidole kava sp. n., Pheidole knowlesi Mann, P. ululevu sp. n., P. vatu Mann, and P. wilsoni Mann. Detailed measurements and descriptions, identification keys, and high-resolution images for queens, major and minor workers are provided. In addition, we include highly detailed 3D surface reconstructions for all available castes.
Project description:Adaptive radiations are of particular interest owing to what they reveal about the ecological and evolutionary regulation of biodiversity. This applies to localized island radiations such as Darwin's finches, and also to rapid radiations occurring on a global scale. Here we analyse the macroevolution and macroecology of Pheidole, a famously hyperdiverse and ecologically dominant ant genus. We generate and analyse four novel datasets: (i) a robust global phylogeny including 285 Pheidole species, (ii) a global database on regional Pheidole richness in 365 political areas summarizing over 97 000 individual records from more than 6500 studies, (iii) a global database of Pheidole richness from 3796 local communities and (iv) a database of Pheidole body sizes across species. Analysis of the potential climate drivers of richness revealed that the patterns are statistically very similar across different biogeographic regions, with both regional and local richness associated with the same coefficients of temperature and precipitation. This similarity occurs even though phylogenetic analysis shows that Pheidole reached dominance in communities through serial localized radiations into different biomes within different continents and islands. Pheidole body size distributions have likewise converged across geographical regions. We propose these cases of convergence indicate that the global radiation of Pheidole is structured by deterministic factors regulating diversification and diversity.
Project description:The evolutionary success of ants and other social insects is considered to be intrinsically linked to division of labor among workers. The role of the brains of individual ants in generating division of labor, however, is poorly understood, as is the degree to which interspecific variation in worker social phenotypes is underscored by functional neurobiological differentiation. Here we demonstrate that dimorphic minor and major workers of different ages from three ecotypical species of the hyperdiverse ant genus Pheidole have distinct patterns of neuropil size variation. Brain subregions involved in sensory input (optic and antennal lobes), sensory integration, learning and memory (mushroom bodies), and motor functions (central body and subesophageal ganglion) vary significantly in relative size, reflecting differential investment in neuropils that likely regulate subcaste- and age-correlated task performance. Worker groups differ in brain size and display patterns of altered isometric and allometric subregion scaling that affect brain architecture independently of brain size variation. In particular, mushroom body size was positively correlated with task plasticity in the context of both age- and subcaste-related polyethism, providing strong, novel support that greater investment in this neuropil increases behavioral flexibility. Our findings reveal striking levels of developmental plasticity and evolutionary flexibility in Pheidole worker neuroanatomy, supporting the hypothesis that mosaic alterations of brain composition contribute to adaptive colony structure and interspecific variation in social organization.
Project description:DNA sequencing is increasingly being used to assist in species identification in order to overcome taxonomic impediment. However, few studies attempt to compare the results of these molecular studies with a more traditional species delineation approach based on morphological characters. Mitochondrial DNA Cytochrome oxidase subunit 1 (CO1) gene was sequenced, measuring 636 base pairs, from 47 ants of the genus Pheidole (Formicidae: Myrmicinae) collected in the Brazilian Atlantic Forest to test whether the morphology-based assignment of individuals into species is supported by DNA-based species delimitation. Twenty morphospecies were identified, whereas the barcoding analysis identified 19 Molecular Operational Taxonomic Units (MOTUs). Fifteen out of the 19 DNA-based clusters allocated, using sequence divergence thresholds of 2% and 3%, matched with morphospecies. Both thresholds yielded the same number of MOTUs. Only one MOTU was successfully identified to species level using the CO1 sequences of Pheidole species already in the Genbank. The average pairwise sequence divergence for all 47 sequences was 19%, ranging between 0-25%. In some cases, however, morphology and molecular based methods differed in their assignment of individuals to morphospecies or MOTUs. The occurrence of distinct mitochondrial lineages within morphological species highlights groups for further detailed genetic and morphological studies, and therefore a pluralistic approach using several methods to understand the taxonomy of difficult lineages is advocated.
Project description:Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown. Phengaris alcon caterpillars undergo particularly dramatic social and dietary shifts when they parasitize Myrmica ant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein-rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities within P. alcon caterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities within P. alcon caterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants (Myrmica schencki), food plant (Gentiana cruciata), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars' surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle of P. alcon caterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development.
Project description:There is a growing recognition that spatial scale is important for understanding ecological processes shaping community membership, but empirical evidence on this topic is still scarce. Ecological processes such as environmental filtering can decrease functional differences among species and promote functional clustering of species assemblages, whereas interspecific competition can do the opposite. These different ecological processes are expected to take place at different spatial scales, with competition being more likely at finer scales and environmental filtering most likely at coarser scales. We used a comprehensive dataset on species assemblages of a dominant ant genus, Pheidole, in the Cerrado (savanna) biodiversity hotspot to ask how functional richness relates to species richness gradients and whether such relationships vary across spatial scales. Functional richness of Pheidole assemblages decreased with increasing species richness, but such relationship did not vary across different spatial scales. Species were more functionally dissimilar at finer spatial scales, and functional richness increased less than expected with increasing species richness. Our results indicate a tighter packing of the functional volume as richness increases and point out to a primary role for environmental filtering in shaping membership of Pheidole assemblages in Neotropical savannas. OPEN RESEARCH BADGES:This article has been awarded Open Materials, Open Data, Preregistered Research Designs Badges. All materials and data are publicly accessible via the Open Science Framework at https://doi.org/10.5061/dryad.31201jg.
Project description:The ability to cultivate food is an innovation that has produced some of the most successful ecological strategies on the planet. Although most well recognized in humans, where agriculture represents a defining feature of civilization, species of ants, beetles, and termites have also independently evolved symbioses with fungi that they cultivate for food. Despite occurring across divergent insect and fungal lineages, the fungivorous niches of these insects are remarkably similar, indicating convergent evolution toward this successful ecological strategy. Here, we characterize the microbiota of ants, beetles, and termites engaged in nutritional symbioses with fungi to define the bacterial groups associated with these prominent herbivores and forest pests. Using culture-independent techniques and the in silico reconstruction of 37 composite genomes of dominant community members, we demonstrate that different insect-fungal symbioses that collectively shape ecosystems worldwide have highly similar bacterial microbiotas comprised primarily of the genera Enterobacter, Rahnella, and Pseudomonas. Although these symbioses span three orders of insects and two phyla of fungi, we show that they are associated with bacteria sharing high whole-genome nucleotide identity. Due to the fine-scale correspondence of the bacterial microbiotas of insects engaged in fungal symbioses, our findings indicate that this represents an example of convergence of entire host-microbe complexes.The cultivation of fungi for food is a behavior that has evolved independently in ants, beetles, and termites and has enabled many species of these insects to become ecologically important and widely distributed herbivores and forest pests. Although the primary fungal cultivars of these insects have been studied for decades, comparatively little is known of their bacterial microbiota. In this study, we show that diverse fungus-growing insects are associated with a common bacterial community composed of the same dominant members. Furthermore, by demonstrating that many of these bacteria have high whole-genome similarity across distantly related insect hosts that reside thousands of miles apart, we show that these bacteria are an important and underappreciated feature of diverse fungus-growing insects. Because of the similarities in the agricultural lifestyles of these insects, this is an example of convergence between both the life histories of the host insects and their symbiotic microbiota.