Amino acid repeats cause extraordinary coding sequence variation in the social amoeba Dictyostelium discoideum.

Protein sequences are normally the most conserved elements of genomes owing to purifying selection to maintain their functions. We document an extraordinary amount of within-species protein sequence variation in the model eukaryote Dictyostelium discoideum stemming from triplet DNA repeats coding for long strings of single amino acids. D. discoideum has a very large number of such strings, many of which are polyglutamine repeats, the same sequence that causes various human neurological disorders in humans, like Huntington's disease. We show here that D. discoideum coding repeat loci are highly variable among individuals, making D. discoideum a candidate for the most variable proteome. The coding repeat loci are not significantly less variable than similar non-coding triplet repeats. This pattern is consistent with these amino-acid repeats being largely non-functional sequences evolving primarily by mutation and drift.

Symbiont fidelity and the origin of species in fungus-growing ants.

A major problem in evolutionary biology is explaining the success of mutualism. Solving this problem requires understanding the level of fidelity between interacting partners. Recent studies have proposed that fungus-growing ants and their fungal cultivars are the products of 'diffuse' coevolution, in which single ant and fungal species are not exclusive to one another. Here we show for ants and associated fungi in the Cyphomyrmex wheeleri species group that each ant species has been exclusively associated with a single fungal cultivar 'species' for millions of years, even though alternative cultivars are readily available, and that rare shifts to new cultivars are associated with ant speciation. Such long-term partner fidelity may have facilitated 'tight' ant-fungus coevolution, and shifts to new fungal cultivars may have had a role in the origin of new ant species.

Phylogeography and sexual macrocyst formation in the social amoeba Dictyostelium giganteum.

BACKGROUND: Microorganisms are ubiquitous, yet we are only beginning to understand their diversity and population structure. Social amoebae (Dictyostelia) are a diverse group of unicellular eukaryotic microbes that display a unique social behaviour upon starvation in which cells congregate and then some die to help others survive and disperse. The genetic relationships among co-occurring cells have a major influence on the evolution of social traits and recent population genetic analysis found extensive genetic variation and possible cryptic speciation in one dictyostelid species (Dictyostelium purpureum). To further characterize the interplay among genetic variation, species boundaries, social behaviour, and reproductive isolation in the Dictyostelia, we conducted phylogenetic analyses and mating experiments with the geographically widespread social amoeba Dictyostelium giganteum. RESULTS: We sequenced approximately 4,000 basepairs of the nuclear ribosomal DNA from 24 isolates collected from Texas, Michigan, Massachusetts, Virginia, and Wisconsin and identified 16 unique haplotypes. Analyses of the sequence data revealed very little genetic differentiation among isolates and no clear evidence of phylogenetic structure, although there was evidence for some genetic differentiation between the Massachusetts and Texas populations. These results suggest that sexual mating (macrocyst formation) is not likely to correlate with either genetic or geographical distance. To test this prediction, we performed 108 mating experiments and found no association between mating probability and genetic or geographical distance. CONCLUSIONS: D. giganteum isolates from across North America display little genetic variation, phylogeographic structure, and genetic differentiation among populations relative to the cryptic species observed within D. purpureum. Furthermore, variation that does exist does not predict the probability of mating among clones. These results have important implications for our understanding of speciation and social evolution in microbes.

Phylogeny, reproductive isolation and kin recognition in the social amoeba Dictyostelium purpureum.

Little is known about the population structure of social microorganisms, yet such studies are particularly interesting for the ways that genetic variation impacts their social evolution. Dictyostelium, a eukaryotic microbe widely used as a developmental model, has a social fruiting stage in which some formerly independent individuals die to help others. To assess genetic variation within the social amoeba Dictyostelium purpureum, we sequenced approximately 4000 base pairs of ribosomal DNA (rDNA) from 37 isolates collected in Texas, Virginia, and Japan. Our analysis showed extensive genetic variation between populations and clear evidence of phylogenetic structure. We identified three major phylogenetic groups that were more different than other accepted species pairs. Tests using pairs of clones showed that both sexual macrocyst and asexual fruiting body formation were influenced by genetic divergence. Macrocysts were less likely to form between pairs of clones from different groups than from the same group. There was also a correlation between the genetic divergence of a pair of clones and their degree of mixing within fruiting bodies. These observations suggest that cryptic species might occur within D. purpureum and, more importantly, reveal how genetic variation impacts social interactions.

Segregate or cooperate- a study of the interaction between two species of Dictyostelium.

BACKGROUND: A major challenge for evolutionary biology is explaining altruism, particularly when it involves death of one party and occurs across species. Chimeric fruiting bodies of Dictyostelium discoideum and Dictyostelium purpureum develop from formerly independent amoebae, and some die to help others. Here we examine co-aggregation between D. discoideum and D. purpureum, determine its frequency and which party benefits, and the extent of fair play in contribution to the altruistic caste. RESULTS: We mixed cells from both species in equal proportions, and then we analyzed 198 individual fruiting bodies, which always had either a D. discoideum or D. purpureum phenotype (D. discoideum- 98, D. purpureum- 100). Fifty percent of the fruiting bodies that looked like D. discoideum and 22% of the fruiting bodies that looked like D. purpureum were chimeric, though the majority of spores in any given fruiting body belonged to one species (D. discoideum fruiting bodies- 0.85 +/- 0.03, D. purpureum fruiting bodies- 0.94 +/- 0.02). Clearly, there is species level recognition occurring that keeps the cells mostly separate. The number of fruiting bodies produced with the D. discoideum phenotype increased from 225 +/- 32 fruiting bodies when D. discoideum was alone to 486 +/- 61 in the mix treatments. However, the number of D. discoideum spores decreased, although not significantly, from 2.75e7 +/- 1.29e7 spores in the controls to 2.06e7 +/- 8.33e6 spores in the mix treatments. D. purpureum fruiting body and spore production decreased from 719 +/- 111 fruiting bodies and 5.81e7 +/- 1.26e7 spores in the controls to 394 +/- 111 fruiting bodies and 9.75e6 +/- 2.25e6 spores in the mix treatments. CONCLUSION: Both species appear to favor clonality but can cooperate with each other to produce fruiting bodies. Cooperating amoebae are able to make larger fruiting bodies, which are advantageous for migration and dispersal, but both species here suffer a cost in producing fewer spores per fruiting body.

High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants.

The control of cheating is important for understanding major transitions in evolution, from the simplest genes to the most complex societies. Cooperative systems can be ruined if cheaters that lower group productivity are able to spread. Kin-selection theory predicts that high genetic relatedness can limit cheating, because separation of cheaters and cooperators limits opportunities to cheat and promotes selection against low-fitness groups of cheaters. Here, we confirm this prediction for the social amoeba Dictyostelium discoideum; relatedness in natural wild groups is so high that socially destructive cheaters should not spread. We illustrate in the laboratory how high relatedness can control a mutant that would destroy cooperation at low relatedness. Finally, we demonstrate that, as predicted, mutant cheaters do not normally harm cooperation in a natural population. Our findings show how altruism is preserved from the disruptive effects of such mutant cheaters and how exceptionally high relatedness among cells is important in promoting the cooperation that underlies multicellular development.

Social evolution: kin preference in a social microbe.

Kin recognition helps cooperation to evolve in many animals, but it is uncertain whether microorganisms can also use it to focus altruistic behaviour on relatives. Here we show that the social amoeba Dictyostelium purpureum prefers to form groups with its own kin in situations where some individuals die to assist others. By directing altruism towards kin, D. purpureum should generally avoid the costs of chimaerism experienced by the related D. discoideum.

Parasitoids and competitors influence colony-level responses in the red imported fire ant, Solenopsis invicta.

Social insect colonies respond to challenges set by a variable environment by re-allocating work among colony members. In many social insects, such colony-level task allocation strategies are achieved through individual decisions that produce a self-organized adapting group. We investigated colony responses to parasitoid and native ant competitors in the red imported fire ant ( Solenopsis invicta). Parasitoid flies affected fire ants by decreasing the proportion of workers engaged in foraging. Competitors also altered colony-level behaviours by reducing the proportion of foraging ants and by increasing the proportion of roaming majors, whose role is colony defence. Interestingly, the presence of both parasitism and competition almost always had similar effects on task allocation in comparison to each of the biotic factors on its own. Thus, our study uniquely demonstrates that the interactive effect of both parasitism and competition is not necessarily additive, implying that these biotic factors alter colony behaviour in distinct ways. More generally, our work demonstrates the importance of studying the dynamics of species interactions in a broader context.

Colony-level impacts of parasitoid flies on fire ants.

The red imported fire ant is becoming a global ecological problem, having invaded the United States, Puerto Rico, New Zealand and, most recently, Australia. In its established areas, this pest is devastating natural biodiversity. Early attempts to halt fire ant expansion with pesticides actually enhanced its spread. Phorid fly parasitoids from South America have now been introduced into the United States as potential biological control agents of the red imported fire ant, but the impact of these flies on fire ant populations is currently unknown. In the laboratory, we show that an average phorid density of as little as one attacking fly per 200 foraging ants decreased colony protein consumption nearly twofold and significantly reduced numbers of large-sized workers 50 days later. The high impact of a single phorid occurred mainly because ants decreased foraging rates in the presence of the flies. Our experiments, the first (to our knowledge) to link indirect and direct effects of phorids on fire ants, demonstrate that colonies can be stressed with surprisingly low parasitoid densities. We interpret our findings with regard to the more complex fire ant-phorid interactions in the field.