Parasite Presence Induces Gene Expression Changes in an Ant Host Related to Immunity and Longevity

Abstract

Most species are either parasites or exploited by parasites, making parasite–host interactions a driver of evolution. Parasites with complex life cycles often evolve strategies to facilitate transmission to the definitive host by manipulating their intermediate host. Such manipulations could explain phenotypic changes in the ant Temnothorax nylanderi, the intermediate host of the cestode Anomotaenia brevis. In addition to behavioral and morphological alterations, infected workers exhibit prolonged lifespans, comparable to that of queens, which live up to two decades. We used transcriptomic data from cestodes and ants of different castes and infection status to investigate the molecular underpinnings of phenotypic alterations in infected workers and explored whether the extended lifespan of queens and infected workers has a common molecular basis. Infected workers and queens commonly upregulated only six genes, one of them with a known anti-aging function. Both groups overexpressed immune genes, although not the same ones. Our findings suggest that the lifespan extension of infected workers is not achieved via the expression of queen-specific genes. The analysis of the cestodes’ transcriptome revealed dominant expression of genes of the mitochondrial respiratory transport chain, which indicates an active metabolism and shedding light on the physiology of the parasite in its cysticercoid stage.

Extreme lifespan extension in tapeworm-infected ant workers

“…Open Sci. 8: 202118 could be activated [30]. Lifespan extension following infection with parasites has been found in other host-parasite systems [20,22,[49][50][51][52].…”

“…Accordingly, the extended lifespan could be caused by the parasite in order to prolong the period of possible transmission. The lifespan extension might be especially feasible in ant workers, which can rely on the care from their nest-mates and where genes for a long life, that is queen-specific genes, could be activated [ 30 ]. Lifespan extension following infection with parasites has been found in other host–parasite systems [ 20 , 22 , 49 – 52 ].…”

“…Infected workers are less active, stay on the brood pile and exhibit reduced flight behaviour [ 23 , 26 ]. These behavioural changes are also reflected in an altered gene expression in the brain and abdomen [ 29 , 30 ].…”

(Epi)Genetic Mechanisms Underlying the Evolutionary Success of Eusocial Insects

“…Infected workers display increased fecundity and longevity comparable to that of a queen, even though they are not of a royal caste [105]. Queens and infected workers share high expression of one known antiaging gene, carboxypeptidase B [106], which has a suggested role in delayed senescence [107]. Enhanced lifespan of infected workers may also be due to overexpression of immunityrelated genes, although there is little overlap between immunity gene expression in queens vs. infected workers [106].…”

“…Queens and infected workers share high expression of one known antiaging gene, carboxypeptidase B [106], which has a suggested role in delayed senescence [107]. Enhanced lifespan of infected workers may also be due to overexpression of immunityrelated genes, although there is little overlap between immunity gene expression in queens vs. infected workers [106]. Future research may benefit from examining the relationship between increased fecundity and longevity in infected workers to better understand the physiological changes that occur when a worker is parasitized.…”