Abstract
Parasitic and symbiotic relationships govern vast nutrient and energy flows, yet controversy surrounds their longevity. Enduring relationships may engender parallel phylogenies among hosts and parasites, but so may ephemeral relationships when parasites colonize related hosts. An understanding of whether symbiont and host populations have grown and contracted in concert would be useful when considering the temporal durability of these relationships. Here, we devised methods to compare demographic histories derived from genomic data. We compared the historical growth of the agent of severe human malaria, Plasmodium falciparum, and its mosquito vector, Anopheles gambiae, to human and primate histories, thereby discerning long-term parallels and anthropogenic population explosions. The growth history of Trichinella spiralis, a zoonotic parasite disseminated by swine, proved regionally specific, paralleling distinctive growth histories for wild boar in Asia and Europe. Parallel histories were inferred for an anemone and its algal symbiont (Exaiptasia pallida and Symbiodinium minutum). Concerted growth in potatoes and the agent of potato blight (Solanum tuberosum and Phytophthora infestans) did not commence until the age of potato domestication. Through these examples, we illustrate the utility of comparative historical demography as a new exploratory tool by which to interrogate the origins and durability of myriad ecological relationships. To facilitate future use of this approach, we introduce a tool called C-PSMC to align and evaluate the similarity of demographic history curves.
Highlights
Symbiotic relationships, including parasitism, are cornerstones of functional ecology, governing vast nutrient and energy flows [1,2]
The demographic history of a population summarizes changes in a multitude of factors, including its census size, sex ratio and gene flow with related populations, which together imprint on the genetic variability of the population
Population genetics measures demography in terms of effective population size (Ne), defined as the minimum census size of an idealized population required for it to harbour the observed level of genetic diversity [6]
Summary
Symbiotic relationships, including parasitism, are cornerstones of functional ecology, governing vast nutrient and energy flows [1,2]. We devised methods to compare and optimally align demographic histories derived from genomic data [9], and applied them to a broad array of parasitic and symbiotic relationships in order to gauge their power to evaluate the origins and temporal durability of such biological dependencies, emphasizing the utility and ease of this novel approach for exploratory analysis and hypothesis generation We used these methods to compare the historical growth of the agent of severe human malaria, Plasmodium falciparum, with human and primate histories [13,14] and with that of their mosquito vector Anopheles gambiae [15], thereby discerning long-term parallels and anthropogenic population explosions [16,17]. The comparison method has been packaged into a software tool called COMPARATIVE PSMC (C-PSMC), which optimally aligns PSMC files in order to score their similarity and estimate relative evolutionary rates
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