Increased genetic diversity from colony merging in termites does not improve survival against a fungal pathogen

Abstract

in some species of social insects the increased genetic diversity from having multiple breeders in a colony has been shown to improve pathogen resistance. termite species typically found colonies from single mated pairs and therefore may lack the flexibility to buffer pathogen pressure with increased genetic diversity by varying the initial number of reproductives. However, they can later increase group diversity through colony merging, resulting in a genetically diverse, yet cohesive, workforce. in this study, we investigate whether the increased group diversity from colony fusion benefits social immunity in the subterranean termite Reticulitermes flavipes. We confirm previous findings that colonies of R. flavipes will readily merge and we show that workers will equally groom nestmates and non-nestmates after merging. Despite this, the survival of these merged colonies was not improved after exposure to a fungal pathogen, but instead leveled to that of the more susceptible or the more resistant colony. our study brings little support to the hypothesis that colony fusion may improve immunity through an increase of genetic diversity in R. flavipes. Instead, we find that following exposure to a lethal pathogen, one colony is heavily influential to the entire group's survival after merging. Social insects are among the most abundant and ecologically successful species 1. Their success is inextricably linked to their division of labor where workers engage in different tasks to benefit one or a few reproductives at the expense of their own reproduction. The low number of reproductives in colonies of most species results in high relatedness among nestmate workers, elevating indirect fitness benefits 2. Paradoxically, their social life also entails severe costs, as high worker densities, high relatedness, and closed nests strongly increase the chance of pathogen transmission, which would suggest that these species are vulnerable to disease outbreaks 3. Owing to such pathogenic pressure, social insects have evolved social immunity, whereby individual immune functions and behaviors collectively provide colony-wide disease protection 4-6. Social immunity includes self/allogrooming 7-14 , nest hygiene 15-22 , removal of diseased individuals 23-26 and the use of antimicrobial compounds either produced by individuals or from materials incorporated into the nest 27-38. These diverse immune strategies have undoubtedly reduced the costs of social living, facilitating the success of social insects. Colony resistance to pathogens is also associated with within-colony genetic diversity, as genetically distinct individuals may vary in their susceptibility to different disease strains 39-45. Therefore, a mix of distinct genotypes within a colony interferes with genotype x genotype interactions, such that a pathogen able to infect one genotype may fail to transmit to new hosts if it encounters host genotypes that it cannot infect. Consequently, a genetically diverse colony may reduce the overall spread of a pathogen. Although variatio...

Natural variation in colony inbreeding does not influence susceptibility to a fungal pathogen in a termite

“…Our results showed no relationship between natural levels of genetic diversity and colony survival against pathogens in R. flavipes colonies. This result is consistent with the absence of improved immunity through increased genetic diversity in artificially mixed colonies of this species (Aguero et al, 2020). It should be noted that the results in this study were obtained when colonies were challenged with only two specific pathogen strains within the same genus.…”

“…Therefore, the reproduction of neotenics extends the life of a colony that would otherwise collapse, at the expense of the colony becoming more inbred over time. Mixed family colonies occur when two separate termite colonies fuse together (Adams et al., 2007; Aguero et al., 2020; Deheer & Kamble, 2008; DeHeer & Vargo, 2004; Fisher et al., 2004; Korb & Schneider, 2007; Perdereau et al., 2010; Thorne et al., 2003). Genetic diversity usually increases in mixed families, depending on the relatedness of the two original colonies.…”

“…In the subterranean termite Reticulitermes flavipes and the dampwood termites of the genus Zootermopsis , colonies can vary dramatically in their susceptibility to different pathogens (Denier & Bulmer, 2015; Rosengaus et al., 2003). However, social immunity of R. flavipes is not improved when genetic diversity is artificially increased by creating mixed families in the laboratory (Aguero et al., 2020). Inbreeding was suggested as one of the numerous factors driving incipient colonies of R. flavipes to collapse, as the proportion of sibling‐founded mature colonies is significantly lower that the proportion of siblings pairing after a mating swarm, suggesting that inbred colonies did not survive over time (DeHeer & Vargo, 2006).…”

Area-Wide Elimination of Subterranean Termite Colonies Using a Novaluron Bait

“…When the primary queen or king dies, nymphs or workers can further develop into neotenic reproductives, which can extend the colony's life span through inbreeding (extended-family colonies) [18][19][20]. Sometimes, distinct colonies can merge into a single genetically diverse, yet cohesive, colony (mixed family) [21]. Overall, these differences in family types may greatly influence the size of the colonies, and consequently their foraging range [19,22].…”

Distinct chemical blends produced by different reproductive castes in the subterranean termite Reticulitermes flavipes

“…Termite colonies were brought back to the lab, removed from their wooden logs and transferred into 10 cm Petri dishes. One worker per colony was sequenced at the mitochondrial 16S gene to confirm species identification, following DNA extraction and sequencing procedures from Aguero et al 71 Only one primary king and two mature (i.e. , fully physogastric) primary queens were found during the sampling.…”