Little to no inbreeding depression in a tapeworm with mixed mating

Abstract

Meta‐studies on hermaphrodites have found a negative relationship between primary selfing rates and levels of inbreeding depression (ID) and, thus, generally support purging in inbred systems. However, in plants, high among‐taxa variance in ID results in no difference in the mean ID between outcrossing and mixed‐mating taxa. Selective interference likely explains high ID among mixed‐mating taxa, whereas low levels of ID among mixed‐mating taxa are not as stressed. Among animal hermaphrodites, primarily molluscs, there are little data on mixed‐mating systems. To fill a taxonomic and mating system gap, we tested for ID in a mixed‐mating tapeworm, Oochoristica javaensis. We provide a direct estimate of ID across infection of an intermediate host by comparing selfing rates at two life history stages. We found little to no evidence for ID, and the level of ID falls in line with what is reported for highly selfing species even though O. javaensis has mixed mating. We discuss this result within the context of kin mating in O. javaensis. Our results emphasize that primary selfing rates alone may be insufficient to classify the inbreeding history in all species when testing for a relationship to ID. Mixed‐mating taxa, and possibly some outcrossing taxa, may exhibit low levels of ID if biparental inbreeding is also driving purging. We advocate that ID studies report estimates of inbreeding history (e.g. FIS or identity disequilibrium) from nature‐derived adult samples to provide context rather than relying on primary selfing rates alone.

Long-term exhaustion of the inbreeding load in Drosophila melanogaster

“…An absence of inbreeding depression among different life-history traits was also found in the ambrosia beetle Xylosandrus germanus (Peer and Taborsky 2005), and for several early fitness traits in a population of the tree Ceiba pentandra, with variable selfing rates among maternal trees (Lobo et al 2015). A reduced inbreeding load (δ = 0.19) was observed in the tapeworm Oochoristica javaensis with mixed mating (Caballero and Criscione 2019) and in the case of the captive population of Cuvier's Gazelle, which showed a positive relationship between juvenile survival and inbreeding (Moreno et al 2015). Other examples of observed reduced or lacking inbreeding depression in wild populations include populations of the lizard Podarcis gaigeae (Runemark et al 2013), the greater white-toothed shrew Crocidura russula (Duarte et al 2003; δ = 0.3 for fecundity), and the invasive biennial Alliaria petiolata (Mullarkey et al 2013).…”

“…Despite the frequent evidence of inbreeding depression in nature, examples can be found in which a reduced population size and high levels of inbreeding do not translate into significant inbreeding depression (e.g., Duarte et al 2003;Laws and Jamieson 2011;Mullarkey et al 2013;Lobo et al 2015;Peer and Taborsky 2005;Runemark et al 2013;Tien et al 2015;Caballero and Criscione 2019). This phenomenon is often explained by the purging of the inbreeding load through the action of natural selection under inbreeding (see, e.g., Hedrick and García-Dorado 2016).…”

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

“…Significantly positive F IS values and deficits of heterozygotes, both indicators of inbreeding, have been detected among cestodes (Lymbery et al 1997), nematodes (Picard et al 2004;Churcher et al 2008), ticks (Dharmarajan et al 2011), and trematodes (Vilas et al 2012). Inbreeding depression has been demonstrated among some tapeworms (Christen et al 2002;Christen and Milinski 2003;Benesh et al 2014), while other species of tapeworm exhibit none, despite high rates of both selfing and sibling mating Caballero and Criscione 2019). By contrast, trematodes infecting salmon (Criscione and Blouin 2006), European conger eel (Vilas and Paniagua 2004), and tapeworms infecting salmonid and coregonid fishes (Šnábel et al 1996), all parasites with complex life cycles and aquatic transmission, appear to outcross whenever possible and self only when hosts are infected with a single individual.…”