The social amoeba Dictyostelium discoideum is a predatory soil protist frequently used for studying host-pathogen interactions. A subset of D. discoideum strains isolated from soil persistently carry ...symbiotic
, recently formally described as
,
, and
. The three facultative symbiont species of D. discoideum present a unique opportunity to study a naturally occurring symbiosis in a laboratory model protist. There is a large difference in genome size between
(8.7 million base pairs Mbp) versus
and
(4.1 Mbp). We took a comparative genomics approach and compared the three genomes of D. discoideum symbionts to 12 additional
genomes to test for genome evolution patterns that frequently accompany host adaptation. Overall,
is difficult to distinguish from other
based on its genome size and content, but the reduced genomes of
and
display characteristics indicative of genome streamlining rather than deterioration during adaptation to their protist hosts. In addition, D. discoideum-symbiont genomes have increased secretion system and motility genes that may mediate interactions with their host. Specifically, adjacent BurBor-like type 3 and T6SS-5-like type 6 secretion system operons shared among all three D. discoideum-symbiont genomes may be important for host interaction. Horizontal transfer of these secretion system operons within the amoeba host environment may have contributed to the unique ability of these symbionts to establish and maintain a symbiotic relationship with D. discoideum.
Protists are a diverse group of typically single cell eukaryotes. Bacteria and archaea that form long-term symbiotic relationships with protists may evolve in additional ways than those in relationships with multicellular eukaryotes such as plants, animals, or fungi. Social amoebas are a predatory soil protist sometimes found with symbiotic bacteria living inside their cells. They present a unique opportunity to explore a naturally occurring symbiosis in a protist frequently used for studying host-pathogen interactions. We show that one amoeba-symbiont species is similar to other related bacteria in genome size and content, while the two reduced-genome-symbiont species show characteristics of genome streamlining rather than deterioration during adaptation to their host. We also identify sets of genes present in all three amoeba-symbiont genomes that are potentially used for host-symbiont interactions. Because the amoeba symbionts are distantly related, the amoeba host environment may be where these genes were shared among symbionts.
When multiple strains of microbes form social groups, such as the multicellular fruiting bodies of Dictyostelium discoideum, conflict can arise regarding cell fate. Both fixed and plastic differences ...among strains can contribute to cell fate, and plastic responses may be particularly important if social environments frequently change. We used RNA‐sequencing and photographic time series analysis to detect possible conflict‐induced plastic differences between wild D. discoideum aggregates formed by single strains compared with mixed pairs of strains (chimeras). We found one hundred and two differentially expressed genes that were enriched for biological processes including cytoskeleton organization and cyclic AMP response (up‐regulated in chimeras), and DNA replication and cell cycle (down‐regulated in chimeras). In addition, our data indicate that in reference to a time series of multicellular development in the laboratory strain AX4, chimeras may be slightly behind clonal aggregates in their development. Finally, phenotypic analysis supported slower splitting of aggregates and a nonsignificant trend for larger group sizes in chimeras. The transcriptomic comparison and phenotypic analyses support discoordination among aggregate group members due to social conflict. These results are consistent with previously observed factors that affect cell fate decision in D. discoideum and provide evidence for plasticity in cAMP signaling and phenotypic coordination during development in response to social conflict in D. discoideum and similar microbial social groups.
When multiple strains of microbes form social groups, such as the multicellular fruiting bodies of social amoebae, evolutionary conflict is expected to arise. We used RNA‐sequencing and photographic time series to detect possible conflict‐induced plastic differences between wild Dictyostelium discoideum aggregates formed by single strains compared with mixed pairs of strains (chimeras). Our results provide evidence for plastic responses in cell signaling and coordination that suggest amoebae can actively respond to the presence of nonrelatives during their single cell to multicellular developmental transition.
Here we give names to three new species of Paraburkholderia that can remain in symbiosis indefinitely in the spores of a soil dwelling eukaryote, Dictyostelium discoideum. The new species P. ...agricolaris sp. nov., P. hayleyella sp. nov., and P. bonniea sp. nov. are widespread across the eastern USA and were isolated as internal symbionts of wild-collected D. discoideum. We describe these sp. nov. using several approaches. Evidence that they are each a distinct new species comes from their phylogenetic position, average nucleotide identity, genome-genome distance, carbon usage, reduced length, cooler optimal growth temperature, metabolic tests, and their previously described ability to invade D. discoideum amoebae and form a symbiotic relationship. All three of these new species facilitate the prolonged carriage of food bacteria by D. discoideum, though they themselves are not food. Further studies of the interactions of these three new species with D. discoideum should be fruitful for understanding the ecology and evolution of symbioses.
In the Allonemobius socius complex of crickets, reproductive isolation is primarily accomplished via postmating prezygotic barriers. We tested seven protein-coding genes expressed in the male ...ejaculate for patterns of evolution consistent with a putative role as postmating prezygotic isolation genes. Our recently diverged species generally lacked sequence variation. As a result, ω-based tests were only mildly successful. Some of our genes showed evidence of elevated ω values on the internal branches of gene trees. In a couple of genes, these internal branches coincided with both species branching events of the species tree, between A. fasciatus and the other two species, and between A. socius and A. sp. nov. Tex. In comparison, more successful approaches were those that took advantage of the varying degrees of lineage sorting and allele sharing among our young species. These approaches were particularly powerful within the contact zone. Among the genes we tested we found genes with genealogies that indicated relatively advanced degrees of lineage sorting across both allopatric and contact zone alleles. Within a contact zone between two members of the species complex, only a subset of genes maintained allelic segregation despite evidence of ongoing gene flow in other genes. The overlap in these analyses was arginine kinase (AK) and apolipoprotein A-1 binding protein (APBP). These genes represent two of the first examples of sperm maturation, capacitation, and motility proteins with fixed non-synonymous substitutions between species-specific alleles that may lead to postmating prezygotic isolation. Both genes express ejaculate proteins transferred to females during copulation and were previously identified through comparative proteomics. We discuss the potential function of these genes in the context of the specific postmating prezygotic isolation phenotype among our species, namely conspecific sperm precedence and the superior ability of conspecific males to induce oviposition in females.
Two of the most well-supported patterns to have emerged over the past two decades of research in evolutionary biology are the occurrence of divergent natural selection acting on many male and female ...reproductive tract proteins and the importance of postmating, prezygotic phenotypes in reproductively isolating closely related species. Although these patterns appear to be common across a wide variety of taxa, the link between them remains poorly documented. Here, we utilize comparative proteomic techniques to determine whether or not there is evidence for natural selection acting on the ejaculate proteomes of two cricket species (Allonemobius fasciatus and A. socius) which are reproductively isolated primarily by postmating, prezygotic phenotypes. In addressing this question, we compare the degree of within-species polymorphism and between-species divergence between the ejaculate and thorax proteomes of these two species. We found that the ejaculate proteomes are both less polymorphic and more divergent than the thorax proteomes. Additionally, we assessed patterns of nucleotide variation for two species-specific ejaculate proteins and found evidence for both reduced levels of variation within species and positive selection driving divergence between species. In contrast, non-species-specific proteins exhibited higher levels of within-species nucleotide variation and no signatures of positive selection. Nucleotide and putative functional data for the two species-specific proteins, along with data for a third protein (ejaculate serine protease), suggest that all three of these genes are candidate speciation genes in need of further study. Overall, these patterns of proteome and nucleotide divergence provide support for the hypothesis that there is a causative link between selection-driven divergence of male ejaculate proteins and the evolution of postmating, prezygotic barriers to gene flow within Allonemobius.
Many microbes engage in social interactions. Some of these have come to play an important role in the study of cooperation and conflict, largely because, unlike most animals, they can be genetically ...manipulated and experimentally evolved. However, whereas animal social behavior can be observed and assessed in natural environments, microbes usually cannot, so we know little about microbial social adaptations in nature. This has led to some difficult-to-resolve controversies about social adaptation even for well-studied traits such as bacterial quorum sensing, siderophore production, and biofilms. Here we use molecular signatures of population genetics and molecular evolution to address controversies over the existence of altruism and cheating in social amoebas. First, we find signatures of rapid adaptive molecular evolution that are consistent with social conflict being a significant force in nature. Second, we find population-genetic signatures of purifying selection to support the hypothesis that the cells that form the sterile stalk evolve primarily through altruistic kin selection rather than through selfish direct reproduction. Our results show how molecular signatures can provide insight into social adaptations that cannot be observed in their natural context, and they support the hypotheses that social amoebas in the wild are both altruists and cheaters.
We investigated field-based recruitment via visual, chemical and acoustic cues provided by conspecific wasps on carbohydrate feeders in Vespula koreensis. A wild colony nest was excavated and ...artificially installed in a field site. Naïve foragers were individually marked and trained to an experimental feeder. We conducted three separate experiments in which foragers were presented with feeder dishes with different cue intensities. For the first, a different number of decoys were posed as if feeding (visual cue). In the second, dishes had been previously visited by different numbers of individuals, thus presenting different concentrations of a possible food site marking substance (chemical cue). In the third, each dish was placed in front of a covered flask with a different number of nestmates inside (acoustic cue combined with body-odor cue). We observed no social facilitation or social inhibition due to any of the experimental cues. Previous studies in Vespula species have shown a variety of foraging strategies ranging from local enhancement to local inhibition. Field-based recruitment mechanisms in yellowjackets may have evolved independently in different lineages.
Understanding how thermal selection affects phenotypic distributions across different time scales will allow us to predict the effect of climate change on the fitness of ectotherms. We tested how ...seasonal temperature variation affects basal levels of cold tolerance and two types of phenotypic plasticity in Drosophila melanogaster. Developmental acclimation occurs as developmental stages of an organism are exposed to seasonal changes in temperature and its effect is irreversible, while reversible short‐term acclimation occurs daily in response to diurnal changes in temperature. We collected wild flies from a temperate population across seasons and measured two cold tolerance metrics (chill‐coma recovery and cold stress survival) and their responses to developmental and short‐term acclimation. Chill‐coma recovery responded to seasonal shifts in temperature, and phenotypic plasticity following both short‐term and developmental acclimation improved cold tolerance. This improvement indicated that both types of plasticity are adaptive, and that plasticity can compensate for genetic variation in basal cold tolerance during warmer parts of the season when flies tend to be less cold tolerant. We also observed a significantly stronger trade‐off between basal cold tolerance and short‐term acclimation during warmer months. For the longer‐term developmental acclimation, a trade‐off persisted regardless of season. A relationship between the two types of plasticity may provide additional insight into why some measures of thermal tolerance are more sensitive to seasonal variation than others.
Our work addresses how genetic variation and phenotypic plasticity, and short‐term (reversible) and developmental (irreversible) acclimation interact to determine the fitness of populations of ectotherms as they respond to seasonal changes in temperature. Using wild Drosophila melanogaster flies collected over multiple seasons and years, we show with lab experiments that phenotypic plasticity can compensate for differences in basal cold tolerance among flies during different seasons. Based on our results, we also predict a constraint between short‐term and developmental acclimation that would influence how well organisms can respond to seasonal variation in a time of climate change.
When species are in intermediate stages of divergence, complicated patterns of reproductive isolation can arise among males and females of the incipient species. The Chrysoperla carnea group of green ...lacewings (Neuroptera: Chrysopidae) has recently experienced rapid speciation. They possess sexually monomorphic mating signals that were assumed to be important in mate recognition. Our objective was to compare patterns of reproductive isolation among five European species within the species complex as well as sex differences in mating strategies that contribute to those patterns. The species were in fact reproductively isolated based on mating signals. In addition, different species showed different degrees of responsiveness to conspecific signals, and those species that responded more frequently to conspecific signals were less discriminating against heterospecific signals. This suggests differences in mating strategies among species that may be related to population densities and heterospecific encounter rates. Sexual dimorphism in mating preference was apparent only in C. agilis, whose males were more responsive to all signals and less discriminating against heterospecific signals compared to females. Thus high variance in male quality may be characteristic of C. agilis, but not the remaining four species, whose male versus female mating strategies were similar.
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