PubMed Health⌕ Search

Biomedical subjects

Ulrich G Mueller

Publications and source records attributed to Ulrich G Mueller.

12 recordsLinked to original sources

Complex host-pathogen coevolution in the Apterostigma fungus-growing ant-microbe symbiosis.

BACKGROUND: The fungus-growing ant-microbe symbiosis consists of coevolving microbial mutualists and pathogens. The diverse fungal lineages that these ants cultivate are attacked by parasitic microfungi of the genus Escovopsis. Previous molecular analyses have demonstrated strong phylogenetic congruence between the ants, the ants-cultivated fungi and the garden pathogen Escovopsis at ancient phylogenetic levels, suggesting coevolution of these symbionts. However, few studies have explored cophylogenetic patterns between these symbionts at the recent phylogenetic levels necessary to address whether these parasites are occasionally switching to novel hosts or whether they are diversifying with their hosts as a consequence of long-term host fidelity. RESULTS: Here, a more extensive phylogenetic analysis of Escovopsis lineages infecting the gardens of Apterostigma ants demonstrates that these pathogens display patterns of phylogenetic congruence with their fungal hosts. Particular clades of Escovopsis track particular clades of cultivated fungi, and closely-related Escovopsis generally infect closely-related hosts. Discordance between host and parasite phylogenies, however, provides the first evidence for occasional host-switches or acquisitions of novel infections from the environment. CONCLUSION: The fungus-growing ant-microbe association has a complex coevolutionary history. Though there is clear evidence of host-specificity on the part of diverse Escovopsis lineages, these pathogens have switched occasionally to novel host fungi. Such switching is likely to have profound effects on how these host and parasites adapt to one another over evolutionary time scales and may impact how disease spreads over ecological time scales.

Agaricales↗

Cryptic sex and many-to-one coevolution in the fungus-growing ant symbiosis.

The fungus-growing ants have long provided a spectacular example of coevolutionary integration. Their ecological success is thought to depend largely on the evolutionary alignment of reproductive interests between ants and fungi after vertical transmission and the ancient suppression of fungal sexuality. In the present study we test these assumptions and provide the first evidence of recombination in attine cultivars, contradicting widely held perceptions of obligate clonality. In addition, we document long-distance horizontal transmission of symbionts between leaf-cutter ant species on mainland Central America and South America and those endemic to Cuba, suggesting both lack of pairwise coevolutionary specificity in ant/cultivar interactions and dispersal of symbionts independent of their ant hosts. The coevolution between leaf-cutters and their fungal symbionts is thus not reciprocally pairwise. Rather, a single widespread and sexual fungal symbiont species is engaged in multiple interactions with divergent ant lineages. Strict fungal clonality and vertical transmission evidently have not played a critical role in the long-term evolutionary or ecological success of this well known mutualism.

Agaricales↗

Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens.

Parasites influence host biology and population structure, and thus shape the evolution of their hosts. Parasites often accelerate the evolution of host defences, including direct defences such as evasion and sanitation and indirect defences such as the management of beneficial microbes that aid in the suppression or removal of pathogens. Fungus-growing ants are doubly burdened by parasites, needing to protect their crops as well as themselves from infection. We show that parasite removal from fungus gardens is more complex than previously realized. In response to infection of their fungal gardens by a specialized virulent parasite, ants gather and compress parasitic spores and hyphae in their infrabuccal pockets, then deposit the resulting pellet in piles near their gardens. We reveal that the ants' infrabuccal pocket functions as a specialized sterilization device, killing spores of the garden parasite Escovopsis. This is apparently achieved through a symbiotic association with actinomycetous bacteria in the infrabuccal pocket that produce antibiotics which inhibit Escovopsis. The use of the infrabuccal pocket as a receptacle to sequester Escovopsis, and as a location for antibiotic administration by the ants' bacterial mutualist, illustrates how the combination of behaviour and microbial symbionts can be a successful defence strategy for hosts.

Actinobacteria↗

Ancient host-pathogen associations maintained by specificity of chemotaxis and antibiosis.

Switching by parasites to novel hosts has profound effects on ecological and evolutionary disease dynamics. Switching requires that parasites are able to establish contact with novel hosts and to overcome host defenses. For most host-parasite associations, it is unclear as to what specific mechanisms prevent infection of novel hosts. Here, we show that parasitic fungal species in the genus Escovopsis, which attack and consume the fungi cultivated by fungus-growing ants, are attracted to their hosts via chemotaxis. This response is host-specific: Escovopsis spp. grow towards their natural host cultivars more rapidly than towards other closely related fungi. Moreover, the cultivated fungi secrete compounds that can suppress Escovopsis growth. These antibiotic defenses are likewise specific: in most interactions, cultivars can inhibit growth of Escovopsis spp. not known to infect them in nature but cannot inhibit isolates of their naturally infecting pathogens. Cases in which cultivars are susceptible to novel Escovopsis are limited to a narrow set of host-parasite strain combinations. Targeted chemotactic and antibiotic responses therefore explain why Escovopsis pathogens do not readily switch to novel hosts, consequently constraining long-term dynamics of host-parasite coevolution within this ancient association.

Animals↗

Exploiting a mutualism: parasite specialization on cultivars within the fungus-growing ant symbiosis.

Fungus-growing ants, their cultivated fungi and the cultivar-attacking parasite Escovopsis coevolve as a complex community. Higher-level phylogenetic congruence of the symbionts suggests specialized long-term associations of host-parasite clades but reveals little about parasite specificity at finer scales of species-species and genotype-genotype interactions. By coupling sequence and amplified fragment length polymorphism genotyping analyses with experimental evidence, we examine (i) the host specificity of Escovopsis strains infecting colonies of three closely related ant species in the genus Cyphomyrmex, and (ii) potential mechanisms constraining the Escovopsis host range. Incongruence of cultivar and ant relationships across the three focal Cyphomyrmex spp. allows us to test whether Escovopsis strains track their cultivar or the ant hosts. Phylogenetic analyses demonstrate that the Escovopsis phylogeny matches the cultivar phylogeny but not the ant phylogeny, indicating that the parasites are cultivar specific. Cross-infection experiments establish that ant gardens can be infected by parasite strains with which they are not typically associated in the field, but that infection is more likely when gardens are inoculated with their typical parasite strains. Thus, Escovopsis specialization is shaped by the parasite's ability to overcome only a narrow range of garden-specific defences, but specialization is probably additionally constrained by ecological factors, including the other symbionts (i.e. ants and their antibiotic-producing bacteria) within the coevolved fungus-growing ant symbiosis.

Analysis of Variance↗

The evolution of cooperation.

Darwin recognized that natural selection could not favor a trait in one species solely for the benefit of another species. The modern, selfish-gene view of the world suggests that cooperation between individuals, whether of the same species or different species, should be especially vulnerable to the evolution of noncooperators. Yet, cooperation is prevalent in nature both within and between species. What special circumstances or mechanisms thus favor cooperation? Currently, evolutionary biology offers a set of disparate explanations, and a general framework for this breadth of models has not emerged. Here, we offer a tripartite structure that links previously disconnected views of cooperation. We distinguish three general models by which cooperation can evolve and be maintained: (i) directed reciprocation--cooperation with individuals who give in return; (ii) shared genes--cooperation with relatives (e.g., kin selection); and (iii) byproduct benefits--cooperation as an incidental consequence of selfish action. Each general model is further subdivided. Several renowned examples of cooperation that have lacked explanation until recently--plant-rhizobium symbioses and bacteria-squid light organs--fit squarely within this framework. Natural systems of cooperation often involve more than one model, and a fruitful direction for future research is to understand how these models interact to maintain cooperation in the long term.

Algorithms↗

Evolution of ant-cultivar specialization and cultivar switching in Apterostigma fungus-growing ants.

Almost all of the more than 200 species of fungus-growing ants (Formicidae: Attini) cultivate litter-decomposing fungi in the family Lepiotaceae (Basidiomycota: Agaricales). The single exception to this rule is a subgroup of ant species within the lower attine genus Apterostigma, which cultivate pterulaceous fungi distantly related to the Lepiotaceae. Comparison of cultivar and ant phylogenies suggests that a switch from lepiotaceous to pterulaceous fungiculture occurred only once in the history of the fungus-growing ants. This unique switch occurred after the origin of the genus Apterostigma, such that the basal Apterostigma lineages retained the ancestral attine condition of lepiotaceous fungiculture, and none of the Apterostigma lineages in the monophyletic group of pterulaceous fungiculturists are known to have reverted back to lepiotaceous fungiculture. The origin of pterulaceous fungiculture in attine ants may have involved a unique transition from the ancestral cultivation of litter-decomposing lepiotaceous fungi to the cultivation of wood-decomposing pterulaceous fungi. Phylogenetic analyses further indicate that distantly related Apterostigma ant species sometimes cultivate the same cultivar lineage, indicating evolutionarily frequent, and possibly ongoing, exchanges of fungal cultivars between Apterostigma ant species. The pterulaceous cultivars form two sister clades, and different Apterostigma ant lineages are invariably associated with, and thus specialized on, only one of the two cultivar clades. However, within clades Apterostigma ant species are able to switch between fungi. This pattern of broad specialization by attine ants on defined cultivar clades, coupled with flexible switching between fungi within cultivar clades, is also found in other attine lineages and appears to be a general phenomenon of fungicultural evolution in all fungus-growing ants.

Adaptation, Physiological↗

The infrabuccal pellet piles of fungus-growing ants.

Fungus-growing ants (Attini) live in an obligate mutualism with the fungi they cultivate for food. Because of the obligate nature of this relationship, the success of the ants is directly dependent on their ability to grow healthy fungus gardens. Attine ants have evolved complex disease management strategies to reduce their garden's exposure to potential parasitic microbes, to prevent the establishment of infection in their gardens, and to remove infected garden sections. The infrabuccal pocket, a filtering device located in the oral cavity of all ants, is an integral part of the mechanisms that leaf-cutter ants use to prevent the invasion and spread of general microbial parasites and the specific fungal-garden parasite Escovopsis. Fungus-growing ants carefully groom their garden, collecting general debris and pathogenic spores of Escovopsis in their infrabuccal pocket, the contents of which are later expelled in dump chambers inside the nest or externally. In this study we examined how a phylogenetically diverse collection of attine ants treat their infrabuccal pellets. Unlike leaf-cutters that deposit their infrabuccal pellets directly in refuse piles, ants of the more basal attine lineages stack their infrabuccal pellets in piles located close to their gardens, and a separate caste of workers is devoted to the construction, management, and eventual disposal of these piles.

Animals↗

Ancient tripartite coevolution in the attine ant-microbe symbiosis.

The symbiosis between fungus-growing ants and the fungi they cultivate for food has been shaped by 50 million years of coevolution. Phylogenetic analyses indicate that this long coevolutionary history includes a third symbiont lineage: specialized microfungal parasites of the ants' fungus gardens. At ancient levels, the phylogenies of the three symbionts are perfectly congruent, revealing that the ant-microbe symbiosis is the product of tripartite coevolution between the farming ants, their cultivars, and the garden parasites. At recent phylogenetic levels, coevolution has been punctuated by occasional host-switching by the parasite, thus intensifying continuous coadaptation between symbionts in a tripartite arms race.

Agaricales↗

Inter-island movements and population differentiation in a pelagic seabird.

We used mark-resight data and amplified fragment length polymorphism (AFLP) markers to assess movements and gene flow between Central Pacific breeding colonies of the great frigatebird, Fregata minor. Of 715 adult frigatebirds marked on Tern Island and Johnston Atoll, 21.3% were resighted at other frigatebird colonies at least 582 km away. Mark-resight data indicated regular movement of males and females between Tern Island and Johnston Atoll (873 km apart), and less frequent movements to other islands; no birds marked on Tern or Johnston were seen on Christmas Island, but one was seen in the Philippines, 7627 km from where it was marked. Despite the regular occurrence of interisland movements, Bayesian analyses of AFLP data showed significant genetic differentiation between Tern Island and Johnston Atoll, and more pronounced differentiation between these two islands and the more distant Christmas Island. The AFLP profiles of three birds breeding on Tern Island fell within the profile-cluster typical for Christmas Island birds, both in a nonmetric multidimensional scaling analysis and in a population assignment test, suggesting dispersal events from Christmas Island to Tern Island. Several factors could explain the persistence of genetic structure despite frequent movements between colonies: many movements occurred during the nonbreeding season, many breeding-season movements did not involve mate-acquisition behaviours and individuals that do disperse may be selected against, as suggested by morphometric differences between colonies. The persistence of genetic structure among breeding colonies despite significant interisland movements suggests limits to the effectiveness of migration as a homogenizing force in this broadly distributed, extremely mobile species.

Animal Migration↗

Fine-scale genetic pattern and evidence for sex-biased dispersal in the túngara frog, Physalaemus pustulosus.

Túngara frogs (Physalaemus pustulosus) are a model system for sexual selection and communication. Population dynamics and gene flow are of major interest in this species because they influence speciation processes and microevolution, and could consequently provide a deeper understanding of the evolutionary processes involved in mate recognition. Although earlier studies have documented genetic variation across the species' range, attempts to investigate dispersal on a local level have been limited to mark-recapture studies. These behavioural studies indicated high mobility at a scale of several hundred metres. In this study we used seven highly polymorphic microsatellite loci to investigate fine-scaled genetic variation in the túngara frog. We analysed the influence of geographical distance on observed genetic patterns, examined the influence of a river on gene flow, and tested for sex-biased dispersal. Data for 668 individuals from 17 populations ranging in distance from 0.26 to 11.8 km revealed significant levels of genetic differentiation among populations. Genetic differentiation was significantly correlated with geographic distance. A river acted as an efficient barrier to gene flow. Several tests of sex-biased dispersal were conducted. Most of them showed no difference between the sexes, but variance of Assignment Indices exhibited a statistically significant male bias in dispersal.

Animals↗