Comparative demography elucidates the longevity of parasitic and symbiotic relationships

Authors: HECHT, LUKE - Oak Ridge Institute For Science And Education (ORISE); THOMPSON, PETER - Oak Ridge Institute For Science And Education (ORISE); Rosenthal, Benjamin

Submitted to: Proceedings of the Royal Society of London: Biological Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/5/2018
Publication Date: 10/3/2018
Citation: Hecht, L.B., Thompson, P.C., Rosenthal, B.M. 2018. Comparative demography elucidates the longevity of parasitic and symbiotic relationships. Proceedings of the Royal Society of London: Biological Sciences. 285:20181032. https://doi.org/10.1098/rspb.2018.1032
DOI: https://doi.org/10.1098/rspb.2018.1032

Interpretive Summary: Although parasitic and symbiotic relationships govern vast nutrient and energy flows through Earth’s ecosystems, controversy surrounds their evolutionary longevity. Enduring relationships engender parallel descent relationships among hosts and parasites, but similar patterns can result, in spite of recurrent host switching, if parasites disproportionately colonize those hosts to which they are most closely related. When considering the durability of such relationships, it would be useful to understand whether parasite and host populations have grown and contracted in concert. Here we found striking correspondence between the growth histories of various parasites with their hosts, and identified strong evidence for explosive growth in the parasites of humans, their pathogens, and those of their crops and livestock since the advent of Agriculture. In a striking counter-example, we identified demographic evidence for the relatively recent origins of potato blight. Comparative historical demography provides a powerful new lens through which to interrogate the history of myriad ecological relationships, enriching our understanding of the origins and durability of important biological relationships. The new approach outined here will be of interest to a broad swath of biologists, including those concerned with the relationships that govern agricultural productivity (such as plant and animal disease, pollinator biology, weed biology) and public health.

Technical Abstract: We sought to determine whether, where, and when contemporaneous population growth and contraction occurred in four parasitic and symbiotic relationships. We first examined the agent of severe human malaria, Plasmodium falciparum, the ancestors of which parasitized non-human primates and presumed to have undergone explosive population growth only after establishing itself in human beings (Joy et al 2003). In this case, we took advantage of high-quality genomic data from human beings and great apes (Pan troglodytes, Gorrilla gorrilla) (Prado-Martinez et al 2013), as well as from this parasite’s Anopheline mosquito vectors (Mongin et al 2002). Secondly, we analyzed the agent of trichinellosis, Trichinella spiralis, a zoonotic nematode parasite whose recent dissemination has been governed by swine domestication and husbandry (Rosenthal et al 2008, Zarlenga 2006); here, we made use of contrasting demographic histories of wild boar in Asia and Europe (Groenen et al 2012) to determine whether corresponding geographic distinctions defined the demographic histories of their parasites. We next sought to determine whether or not participants in a marine symbiosis, known to be influenced by climate variation, have had a discernibly parallel history of population growth and contraction: the anemone Aiptasia pallida (Baumgarten et al 2015) and its photosynthetic algal symbiont Symbiodinium minutum (Shoguchi et al 2013). Finally, we considered the fungal agent of potato blight, Phytophthora infestans (Haas et al 2009), in relation to the history of potatoes (Solanum tuberosum) (Consortium Potato Genome 2011), suspecting that this association may have been established from an evolutionarily recent host shift. Distinctions among the demographic histories of our various systems pervaded until the Anthropocene, when human beings and our domesticated livestock and crops engendered population explosions in our pathogens and those of our domesticates.