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1. Gene flow accelerates adaptation to a parasite

   https://doi.org/10.1093/evolut/qpad048  

   Lewis, Jordan A; Kandala, Prathyusha; Penley, Mc Kenna; Morran, Levi T (March 2023, Evolution)

   Abstract Gene flow into populations can increase additive genetic variation and introduce novel beneficial alleles, thus facilitating adaptation. However, gene flow may also impede adaptation by disrupting beneficial genotypes, introducing deleterious alleles, or creating novel dominant negative interactions. While theory and fieldwork have provided insight as to the effects of gene flow, direct experimental tests are rare. Here, we evaluated the effects of gene flow on adaptation in the nematode Caenorhabditis elegans during exposure to the bacterial parasite Serratia marcescens. We evolved hosts against non-evolving parasites for ten passages while controlling host gene flow and source population. We used source nematode populations with three different genetic backgrounds (one similar to the sink population and two different) and two evolutionary histories (previously adapted to S. marcescens or naïve). We found that populations with gene flow exhibited greater increases in parasite resistance than those without gene flow. Additionally, gene flow from adapted populations resulted in greater increases in resistance than gene flow from naïve populations, particularly with gene flow from novel genetic backgrounds. Overall, this work demonstrates that gene flow can facilitate adaptation, and suggests that the genetic architecture and evolutionary history of source populations can alter the sink population’s response to selection. 

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2. Genomics of sorghum local adaptation to a parasitic plant

   https://doi.org/10.1073/pnas.1908707117  

   Bellis, Emily S.; Kelly, Elizabeth A.; Lorts, Claire M.; Gao, Huirong; DeLeo, Victoria L.; Rouhan, Germinal; Budden, Andrew; Bhaskara, Govinal B.; Hu, Zhenbin; Muscarella, Robert; et al (February 2020, Proceedings of the National Academy of Sciences)

   Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica -prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit of LGS1 -mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities. 

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3. How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale?

   https://doi.org/10.1007/s00265-021-03089-y  

   Janecka, Mary J.; Rovenolt, Faith; Stephenson, Jessica F. (November 2021, Behavioral Ecology and Sociobiology)

   Social interactions with conspecifics are key to the fitness of most animals and, through the transmission opportunities they provide, are also key to the fitness of their parasites. As a result, research to date has largely focused on the role of host social behavior in imposing selection on parasites, particularly their virulence and transmission phenotypes. However, host social behavior also influences the distribution of parasites among hosts, with implications for their evolution through non-random mating, gene flow, and genetic drift, and thus ability to respond to that selection. Here, we review the paucity of empirical studies on parasites, and draw from empirical studies of free-living organisms and population genetic theory to propose several mechanisms by which host social behavior potentially drives parasite evolution through these less-well studied mechanisms. We focus on the guppy host and Gyrodactylus (Monogenea) ectoparasitic flatworm system and follow a spatially hierarchical outline to highlight that social behavior varies between individuals, and between host populations across the landscape, generating a mosaic of ecological and evolutionary outcomes for their infecting parasites. We argue that the guppy-Gyrodactylus system presents a unique opportunity to address this fundamental knowledge gap in our understanding of the connection between host social behavior and parasite evolution. Individual differences in host social behavior generates fine-scale changes in the spatial distribution of parasite genotypes, shape the size, and diversity of their infecting parasite populations and may generate non-random mating on, and non-random transmission between hosts. While at population and metapopulation level, variation in host social behavior interacts with landscape structure to affect parasite gene flow, effective population size, and genetic drift to alter the coevolutionary potential of local adaptation. 

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4. The pan-genome of Aspergillus fumigatus provides a high-resolution view of its population structure revealing high levels of lineage-specific diversity driven by recombination

   https://doi.org/10.1371/journal.pbio.3001890  

   Lofgren, Lotus A.; Ross, Brandon S.; Cramer, Robert A.; Stajich, Jason E. (November 2022, PLOS Biology)

   Sil, Anita (Ed.)

   Aspergillus fumigatus is a deadly agent of human fungal disease where virulence heterogeneity is thought to be at least partially structured by genetic variation between strains. While population genomic analyses based on reference genome alignments offer valuable insights into how gene variants are distributed across populations, these approaches fail to capture intraspecific variation in genes absent from the reference genome. Pan-genomic analyses based on de novo assemblies offer a promising alternative to reference-based genomics with the potential to address the full genetic repertoire of a species. Here, we evaluate 260 genome sequences of A . fumigatus including 62 newly sequenced strains, using a combination of population genomics, phylogenomics, and pan-genomics. Our results offer a high-resolution assessment of population structure and recombination frequency, phylogenetically structured gene presence–absence variation, evidence for metabolic specificity, and the distribution of putative antifungal resistance genes. Although A . fumigatus disperses primarily via asexual conidia, we identified extraordinarily high levels of recombination with the lowest linkage disequilibrium decay value reported for any fungal species to date. We provide evidence for 3 primary populations of A . fumigatus , with recombination occurring only rarely between populations and often within them. These 3 populations are structured by both gene variation and distinct patterns of gene presence–absence with unique suites of accessory genes present exclusively in each clade. Accessory genes displayed functional enrichment for nitrogen and carbohydrate metabolism suggesting that populations may be stratified by environmental niche specialization. Similarly, the distribution of antifungal resistance genes and resistance alleles were often structured by phylogeny. Altogether, the pan-genome of A . fumigatus represents one of the largest fungal pan-genomes reported to date including many genes unrepresented in the Af293 reference genome. These results highlight the inadequacy of relying on a single-reference genome-based approach for evaluating intraspecific variation and the power of combined genomic approaches to elucidate population structure, genetic diversity, and putative ecological drivers of clinically relevant fungi. 

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5. Causation without correlation: parasite-mediated frequency-dependent selection and infection prevalence

   https://doi.org/10.1098/rsbl.2021.0321  

   Lively, Curtis M.; Xu, Julie; Ben-Ami, Frida (December 2021, Biology Letters)

   Parasite-mediated selection is thought to maintain host genetic diversity for resistance. We might thus expect to find a strong positive correlation between host genetic diversity and infection prevalence across natural populations. Here, we used computer simulations to examine host–parasite coevolution in 20 simi-isolated clonal populations across a broad range of values for both parasite virulence and parasite fecundity. We found that the correlation between host genetic diversity and infection prevalence can be significantly positive for intermediate values of parasite virulence and fecundity. But the correlation can also be weak and statistically non-significant, even when parasite-mediated frequency-dependent selection is the sole force maintaining host diversity. Hence correlational analyses of field populations, while useful, might underestimate the role of parasites in maintaining host diversity. 

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