Clonemate cotransmission supports a role for kin selection in a puppeteer parasite

Abstract

Host manipulation by parasites is a fascinating evolutionary outcome, but adaptive scenarios that often accompany even iconic examples in this popular field of study are speculative. Kin selection has been invoked as a means of explaining the evolution of an altruistic-based, host-manipulating behavior caused by larvae of the lancet flukeDicrocoelium dendriticumin ants. Specifically, cotransmission of larval clonemates from a snail first host to an ant second host is presumed to lead to a puppeteer parasite in the ant’s brain that has clonemates in the ant abdomen. Clonal relatedness between the actor (brain fluke) and recipients (abdomen flukes) enables kin selection of the parasite’s host-manipulating trait, which facilitates transmission of the recipients to the final host. However, the hypothesis that asexual reproduction in the snail leads to a high abundance of clonemates in the same ant is untested. Clonal relationships between the manipulator in the brain and the nonmanipulators in the abdomen are also untested. We provide empirical data on the lancet fluke’s clonal diversity within its ant host. In stark contrast to other trematodes, which do not exhibit the same host-manipulating behavioral trait, the lancet fluke has a high abundance of clonemates. Moreover, our data support existing theory that indicates that the altruistic behavior can evolve even in the presence of multiple clones within the same ant host. Importantly, our analyses conclusively show clonemate cotransmission into ants, and, as such, we find support for kin selection to drive the evolution and maintenance of this iconic host manipulation.

Evidence of population structuring following population genetic analyses of Fasciola hepatica from Argentina

“…We identified genetically identical parasites (clones) in 12 of 14 definitive hosts studied, a finding consistent with previous studies in livestock, where 61% and 85% of hosts studied contained genetically identical parasites ( Vilas et al, 2012 , Beesley et al, 2017 ). This supports the theory that following clonal expansion within the snail, there is some co-transmission of clonemates to the definitive host, similar to previous reports ( Beesley et al, 2017 ), but does not extend to the low clonal diversity observed in sheep for F. hepatica ( Vilas et al, 2012 ), and it does not occur to the same extent as clonemate co-transmission recently observed for D. dendriticum ( Criscione et al, 2020 ).…”

“…A recent study in the trematode Dicrocoelium dendriticum (land snail-ant-ungulate) revealed the lowest clonal diversity for any trematode to date, with only 54 of 272 (19.9%) genotypes being unique. This observation was consistent with the restricted movements of the snails and ants under investigation, and the likely localised adherence of the slime balls, containing the cercariae, that infect the ant ( Criscione et al, 2020 ). Appreciating the geographical scale over which studies are conducted facilitates their interpretation.…”

“…This agrees with previous findings of up to nine or 10 parasites with the same genotype ( Vilas et al, 2012 , Beesley et al, 2017 ), and has also been reported in Fascioloides magna, where nine parasites in one deer had the same five locus allozyme genotype ( Mulvey et al, 1991 ). Within D. dendriticum, up to 22 parasites shared the same genotype in the second intermediate ant host ( Criscione et al, 2020 ). However, in S. mansoni the mean number of copies of a clone was 3.15 (standard error ± 0.47; Prugnolle et al, 2004 ), and findings from aquatic trematodes usually report a maximum of two to four copies of each clone ( Rauch et al, 2005 , Criscione and Blouin, 2006 , Keeney et al, 2007a , Lagrue et al, 2009 , Leung et al, 2009 , Valdivia et al, 2014 ).…”

Genetic architecture of transmission stage production and virulence in schistosome parasites

“…Parasites face a central problem: how to maximize transmission to the next host. This has driven the evolution of a wide variety of lifecycle features to facilitate parasite transmission [ 1 , 2 ]. However, perhaps the most common transmission strategy is to produce vast numbers of infective stages [ 3 , p. 20].…”

Genetic architecture of transmission stage production and virulence in schistosome parasites

“…Parasites face a central problem: how to maximize transmission to the next host. This has driven the evolution of a wide variety of lifecycle features to facilitate parasite transmission (Criscione et al, 2020;Vasudevan et al, 2015). However, perhaps the most common transmission strategy is to produce vast numbers of infective stages (Loker and Hofkin, 2015, p. 20).…”