skip to main content


Title: Genomic evidence for population‐specific responses to co‐evolving parasites in a New Zealand freshwater snail
Abstract

Reciprocal co‐evolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population‐ or genotype‐specific evolutionary change. These host–parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of co‐evolving host–parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snailPotamopyrgus antipodarumand its co‐evolving sterilizing trematode parasite,Microphallussp., a textbook example of natural coevolution. We found thatMicrophallus‐infectedP. antipodarumexhibit systematic downregulation of genes relative to uninfectedP. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population‐level co‐evolution is leading to population‐specific host–parasite interactions and evolutionary trajectories. We also used anFST‐based approach to identify a set of loci that represent promising candidates for targets of parasite‐mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population‐specific responses to co‐evolving infection in theP. antipodarum‐Microphallusinteraction and provide new insights into the genomic basis of co‐evolutionary interactions in nature.

 
more » « less
PAR ID:
10035641
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
26
Issue:
14
ISSN:
0962-1083
Page Range / eLocation ID:
p. 3663-3675
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Host–parasite interactions may often be subject to opposing evolutionary forces, which likely influence the evolutionary trajectories of both partners. Natural selection and genetic drift are two major evolutionary forces that act in host and parasite populations. Further, population size is a significant determinant of the relative strengths of these forces. In small populations, drift may undermine the persistence of beneficial alleles, potentially impeding host adaptation to parasites. Here, we investigate two questions: (a) can selection pressure for increased resistance in small, susceptible host populations overcome the effects of drift and (b) can resistance be maintained in small host populations? To answer these questions, we experimentally evolved the hostCaenorhabditis elegansagainst its bacterial parasite,Serratia marcescens, for 13 host generations. We found that strong selection favouring increased host resistance was insufficient to counteract drift in small populations, resulting in persistently high host mortality. Additionally, in small populations of resistant hosts, we found that selection for the maintenance of resistance is not always sufficient to curb the loss of resistance. We compared these results with selection in large host populations. We found that initially resistant, large host populations were able to maintain high levels of resistance. Likewise, initially susceptible, large host populations were able to gain resistance to the parasite. These results show that strong selection pressure for survival is not always sufficient to counteract drift. In consideration ofC.elegans natural population dynamics, we suggest that drift may often impede selection in nature.

     
    more » « less
  2. Abstract

    Understanding both sides of host–parasite relationships can provide more complete insights into host and parasite biology in natural systems. For example, phylogenetic and population genetic comparisons between a group of hosts and their closely associated parasites can reveal patterns of host dispersal, interspecies interactions, and population structure that might not be evident from host data alone. These comparisons are also useful for understanding factors that drive host–parasite coevolutionary patterns (e.g., codivergence or host switching) over different periods of time. However, few studies have compared the evolutionary histories between multiple groups of parasites from the same group of hosts at a regional geographic scale. Here, we used genomic data to compare phylogenomic and population genomic patterns of Alaska ptarmigan and grouse species (Aves: Tetraoninae) and two genera of their associated feather lice:LagopoecusandGoniodes. We used whole‐genome sequencing to obtain hundreds of genes and thousands of single‐nucleotide polymorphisms (SNPs) for the lice and double‐digest restriction‐associated DNA sequences to obtain SNPs from Alaska populations of two species of ptarmigan. We found that both genera of lice have some codivergence with their galliform hosts, but these relationships are primarily characterized by host switching and phylogenetic incongruence. Population structure was also uncorrelated between the hosts and lice. These patterns suggest that grouse, and ptarmigan in particular, share habitats and have likely had historical and ongoing dispersal within Alaska. However, the two genera of lice also have sufficient dissimilarities in the relationships with their hosts to suggest there are other factors, such as differences in louse dispersal ability, that shape the evolutionary patterns with their hosts.

     
    more » « less
  3. Abstract Background

    Experimental evolution has a long history of uncovering fundamental insights into evolutionary processes, but has largely neglected one underappreciated component--the microbiome. As eukaryotic hosts evolve, the microbiome may also respond to selection. However, the microbial contribution to host evolution remains poorly understood. Here, we re-analyzed genomic data to characterize the metagenomes from ten Evolve and Resequence (E&R) experiments inDrosophila melanogasterto determine how the microbiome changed in response to host selection.

    Results

    Bacterial diversity was significantly different in 5/10 studies, primarily in traits associated with metabolism or immunity. Duration of selection did not significantly influence bacterial diversity, highlighting the importance of associations with specific host traits.

    Conclusions

    Our genomic re-analysis suggests the microbiome often responds to host selection; thus, the microbiome may contribute to the response ofDrosophilain E&R experiments. We outline important considerations for incorporating the microbiome into E&R experiments. The E&R approach may provide critical insights into host-microbiome interactions and fundamental insight into the genomic basis of adaptation.

     
    more » « less
  4. Abstract Host-specific interactions can maintain genetic and phenotypic diversity in parasites that attack multiple host species. Host diversity, in turn, may promote parasite diversity by selection for genetic divergence or plastic responses to host type. The parasitic weed purple witchweed [ Striga hermonthica (Delile) Benth.] causes devastating crop losses in sub-Saharan Africa and is capable of infesting a wide range of grass hosts. Despite some evidence for host adaptation and host-by- Striga genotype interactions, little is known about intraspecific Striga genomic diversity. Here we present a study of transcriptomic diversity in populations of S. hermonthica growing on different hosts (maize [ Zea mays L.] vs. grain sorghum [ Sorghum bicolor (L.) Moench]). We examined gene expression variation and differences in allelic frequency in expressed genes of aboveground tissues from populations in western Nigeria parasitizing each host. Despite low levels of host-based genome-wide differentiation, we identified a set of parasite transcripts specifically associated with each host. Parasite genes in several different functional categories implicated as important in host–parasite interactions differed in expression level and allele on different hosts, including genes involved in nutrient transport, defense and pathogenesis, and plant hormone response. Overall, we provide a set of candidate transcripts that demonstrate host-specific interactions in vegetative tissues of the emerged parasite S. hermonthica . Our study shows how signals of host-specific processes can be detected aboveground, expanding the focus of host–parasite interactions beyond the haustorial connection. 
    more » « less
  5. Abstract

    The extent and magnitude of parasitism often vary among closely related host species and across populations within species. Determining the ecological basis for this species and population‐level variation in parasitism is critical for understanding infection dynamics in multi‐host–parasite systems. To investigate such ecological underpinnings of variation in parasitism, we studiedEnallagmadamselfly host species and their water mite (Arrenurusspp.) ectoparasites in lakes.

    We first evaluated how host identity and density could shape parasitism. To test the effects of con‐ and heterospecific host density on parasitism, we used a field experiment withEnallagma basidensandE. signatum. We found that parasitism did not vary with con‐ or heterospecific density and was determined by host identity alone, with no spillover effects.

    We also evaluated the potential role of local adaptation and resource availability in shaping parasitism. To do so, we usedE. signatumin a reciprocal transplant experiment crossed with a prey resource‐level manipulation. This experiment revealed that parasitism declined sharply for one host population in its non‐local lake, but not the other source population, with no effects of prey levels. This asymmetry implies that damselflies express enhanced defences against parasitism that are neither population‐specific nor dependent on resource abundance, or that mites developed heightened local host specificity.

    The results of multivariate modeling from an observational study generally supported these experimental findings: neither host density nor resource abundance strongly explained among‐population variation in parasitism. Instead, local abiotic conditions (pH) had the strongest relationship with parasitism, with minimal associations with predator density, temperature and a measure of immune function.

    Collectively, our findings suggest a crucial role for the local environment in shaping host–parasite interactions within multi‐host–parasite systems. More generally, these results show that research at the intersection of community ecology and disease ecology is critical for understanding host–parasite dynamics within natural communities.

     
    more » « less