A phylogenetic test of the Red Queen Hypothesis: Outcrossing and parasitism in the Nematode phylum

Abstract

Sexual outcrossing is costly relative to selfing and asexuality, yet it is ubiquitous in nature, a paradox that has long puzzled evolutionary biologists. The Red Queen Hypothesis argues that outcrossing is maintained by antagonistic interactions between host and parasites. Most tests of this hypothesis focus on the maintenance of outcrossing in hosts. The Red Queen makes an additional prediction that parasitic taxa are more likely to be outcrossing than their free-living relatives. We test this prediction in the diverse Nematode phylum using phylogenetic comparative methods to evaluate trait correlations. In support of the Red Queen, we demonstrate a significant correlation between parasitism and outcrossing in this clade. We find that this correlation is driven by animal parasites, for which outcrossing is significantly enriched relative to both free-living and plant parasitic taxa. Finally, we test hypotheses for the evolutionary history underlying the correlation of outcrossing and animal parasitism. Our results demonstrate that selfing and asexuality are significantly less likely to arise on parasitic lineages than on free-living ones. The findings of this study are consistent with the Red Queen Hypothesis. Moreover, they suggest that the maintenance of genetic variation is an important factor in the persistence of parasitic lineages.

Parthenogenetic vs. sexual reproduction in oribatid mite communities

“…It therefore predicts sexual taxa to dominate in habitats where parasite-host and/ or predator-prey interactions control community dynamics (Hamilton, 1980;Jaenike, 1978), which is often the case when predators/ parasites reach high densities (Ladle, 1992). A number of field and laboratory studies supported the RQT (Gibson & Fuentes, 2015;Haafke, Chakra, & Becks, 2016;Kotusz et al, 2014), but many are based on a single parasite-host system, the snail Potamogyrgus antipodarum and its trematode parasite (Jokela, Dybdahl, & Lively, 2009;King, Delph, Jokela, & Lively, 2009;Lively, 2010). A number of field and laboratory studies supported the RQT (Gibson & Fuentes, 2015;Haafke, Chakra, & Becks, 2016;Kotusz et al, 2014), but many are based on a single parasite-host system, the snail Potamogyrgus antipodarum and its trematode parasite (Jokela, Dybdahl, & Lively, 2009;King, Delph, Jokela, & Lively, 2009;Lively, 2010).…”

“…The RQT does not make explicit predictions on the effects of resource availability, but it has been suggested that small populations are less infested by parasites (Arneberg, Skorping, Grenfell, & Read, 1998) thereby weakening Red Queen processes. A number of field and laboratory studies supported the RQT (Gibson & Fuentes, 2015;Haafke, Chakra, & Becks, 2016;Kotusz et al, 2014), but many are based on a single parasite-host system, the snail Potamogyrgus antipodarum and its trematode parasite (Jokela, Dybdahl, & Lively, 2009;King, Delph, Jokela, & Lively, 2009;Lively, 2010).…”

Assortative mating and self-fertilization differ in their contributions to reinforcement, cascade speciation, and diversification

“…We evaluated if uniparental reproduction is associated with lower or higher diversification rates. Taxa were classified following Gibson and Fuentes (2015) , in which male frequency was used as a proxy for mating system. Because the absence of males cannot distinguish parthenogenesis (asexuality) from androdioecy (mostly selfing), these two modes are treated as a single category of uniparental reproduction.…”

“…We used the phylogeny and character data originally reported in Gibson and Fuentes (2015) , which included a phylogenetic reconstruction of 2,700 postburn-in trees modified from Meldal et al. (2007) .…”

A Model for Evolutionary Ecology of Disease: The Case for Caenorhabditis Nematodes and Their Natural Parasites

“…The topic of mating system evolution continually arises with the caenorhabditids, and with nematodes more in general. Mating system varies throughout the entire phylum, from obligate outcrossing to selfing to parthenogenesis (Bell, 1982;Denver et al, 2011;Gibson and Fuentes, 2015). Within the caenorhabditids, selfing has evolved multiple times from the ancestral state of obligate outcrossing (Kiontke et al, 2004;Kiontke and Fitch, 2005;Cutter et al, 2008).…”