Short and long-term costs of inbreeding in the lifelong-partnership in a termite

Pierre-André Eyer^*, Edward L. Vargo

Department of Entomology, 2143 TAMU, Texas A&M University, College Station, Texas, 77843-2143, USA

Running title: Costs of inbreeding in termite colonies

Type of article: Letter

Number of words: Abstract: 144, Main text: 5150, Box: 0.

Number of references: 91

Number of figures: 6, Tables: 0, Box: 0.

^*Correspondence

Pierre-André Eyer

Department of Entomology,

Texas A&M University,

College Station, 77843, Texas, USA

e-mail: pieyer@live.fr

ABSTRACT

Social life and lifelong partner commitments are expected to favor thorough partner choice, as an ill-suited partnership may have long-term consequences, adversely affecting the parents and spanning several cohorts of offspring. Here, we used ~1400 termite incipient colonies to estimate the short- and long-term costs of inbreeding upon the survival of the parents over a 15-month period, their productivity, and the resistance of their offspring toward pathogen pressure. We observed that foundation success was not influenced by the relatedness of partners, but by their levels of microbial load. We showed faster growth in inbred colonies, revealing a potential tradeoff with pathogen susceptibility. Yet, inbreeding takes its toll later in colony development when incipient colonies face pathogen pressure. Although the consequences of choosing a lifetime partner is initially determined by the partner’s health, the cost of inbreeding in incipient colonies favors outbred colonies reaching maturity.

SHORT ABSTRACT

We used termite colonies to study the short- and long-term costs of inbreeding on the survival of the parents, their productivity and their offspring survival toward pathogens. Colony founding success was not influenced by relatedness of partners, but by their microbial load, yet inbreeding may make small colonies more susceptible to pathogens. Lifelong partner commitment is first affected by the immediate benefit of a healthy partner, inbreeding depression restores outbreeding in mature colonies.

INTRODUCTION

The difference between the sexes in their gamete and offspring investment generally leads to females being considered the choosy sex and males the more promiscuous sex. However, in high fidelity species, epitomized by the social Hymenoptera where males live as stored sperm, a detrimental mating cannot be remedied by new reproductive events. Lifelong partner commitments are expected to favor extreme choosiness by both sexes (Shellman-Reeve 1999; Boomsma 2013). Additionally, the consequences of poor mate choice are higher for social species as the parents may be adversely affected, since they rely on their offspring for care, not only for themselves but also for rearing their future brood. Therefore, an ill-suited partnership may have long-term consequences, spanning several cohorts of offspring.

Mating with close relatives is commonly seen as detrimental due to the deleterious consequences of inbreeding, which logically suggests that evolution favors mechanisms preventing its occurrence (Nichols 2017). Particularly well-studied in social and/or monogamous groups, inbreeding avoidance may arise through increased dispersal, reducing the likelihood of encountering relatives (Clutton-Brock 1989), or through delayed reproduction via parental inhibition, preventing mating between the parents and their offspring (Wolff 1992; Abbott 1993). Remarkably, this sexual repression is lost when the opposite-sex parent is absent or replaced (Hanby & Bygott 1987; Koenig WD et al. 1998). Inbreeding may also be reduced through extra-group fertilizations, whereby offspring are not fathered by the males in their group, despite caring for the offspring (Brooked et al. 1990; Amos et al.1993; Sillero-Zubiri et al. 1996). Finally, inbreeding avoidance may occur through recognition and avoidance of kin matings (Blouin & Blouin 1988; Pusey & Wolf 1996; Gerlach & Lysiak 2006). In some cases, the scent of related males is unattractive and may even inhibit sexual behavior in their female relatives (Hurst et al. 2001).

Termites are eusocial insects that usually establish their colonies through the pairing of a winged queen and king (Vargo & Husseneder 2011). The royal couple spends their entire lives together secluded within colonies, therefore usually preventing extra-pair fertilizations (colony fusion may allow extra-pair fertilizations in rare cases). During colony foundation, the queen and king frequently engage in social interactions, such as grooming and trophallactic exchanges (Shellman-Reeve 1990), and founding success is directly tied to the health of each partner (Cole et al. 2018). The absence of workers prevents founding colonies from reaping the full benefits of social immunity, as workers collectively enhance disease resistance through the maintenance of nest hygiene, allogrooming and the exchange of antimicrobial substances (Traniello et al. 2002; Cremer et al. 2007; Rosengaus et al. 2011b). In incipient colonies, the parents’ limited resources are drained by the production and care of the first brood, which is altricial for the two first instars which are more susceptible to pathogens than older workers (Rosengaus & Traniello 2001; Cole et al. 2018; Cole et al. 2020). Success of incipient colonies therefore increases with the body size of the founders and their contribution to biparental care (Cole et al.2018; Chouvenc 2019; Cole & Rosengaus 2019). However, as the colony grows, brood care, food foraging and immune maintenance are undertaken by older workers, whereas the queen and king forego their parental duties to specialize in reproduction (Matsuura & Kobayashi 2010). These behavioral and physiological changes highlight the importance of both partners and their mutual compatibility in the success of incipient colonies. They also emphasize the changing roles queens and kings play within colonies, questioning whether these different pressures influence selection for distinct partner traits over the lifespan of a colony.

Several lines of evidence suggest that inbreeding hampers the development of termite colonies. In Zootermopsis angusticollis , inbred groups are more susceptible toward a fungal pathogen and exhibit higher cuticular microbial loads, potentially resulting from less effective allogrooming (Calleri et al. 2006). InReticulitermes flavipes, a high proportion of reproductives pair up with nestmates during the nuptial flight (25%); yet this proportion is reduced among established colonies, suggesting that inbreeding negatively affects colony development (DeHeer & Vargo 2006). However, the susceptibility of mature colonies toward pathogens was not found to be associated with their level of inbreeding (Aguero et al.2021b); rather, specific genetic backgrounds seem to determine their survival to a greater extent than overall genetic diversity. Similarly, increased diversity from colony fusion was not found to improve survival toward pathogens. Merged colony survival was instead equal to that of either the more susceptible or the more resistant colony, highlighting the complementary roles of both colonies of origin (Aguero et al.2020). Similarly, inbreeding does not seem detrimental during colony establishment in Z. angusticollis and offspring production was reported to be similar between inbred and outbred pairings. However, the survival of incipient colonies was remarkably higher when initiated by inbred reproductives, which the authors suggested likely resulted from the immune priming of nestmate reproductives toward familiarpathogens due to prior exposure within their natal colony (Rosengaus & Traniello 1993). In contrast, high mortality in outbred pairings may stem from non-nestmates facing naïve pathogens carried by their partner, toward which they may be more vulnerable (Rosengaus & Traniello 1993).

Here, we sought to untangle the complex interaction between inbreeding and pathogen pressure on colony foundation in termites[, ]. Using six stock colonies of R. flavipes (Perdereau et al. 2013; Eyer et al. 2021a), we set up inbred and outbred pairings. We first investigated the short-term cost of outbreeding by assessing the influence of genetic relatedness, microbial loads and microbial similarities on foundation success over the first 14 days. Second, we investigated the long-term cost of inbreeding by comparing inbred and outbred pairings over a 15-month period for their survival, their productivity (worker and soldier), and the resistance of their offspring toward entomopathogenic pressure. Overall, we show that inbreeding and outbreeding entail different costs at distinct stages of a colony’s lifespan; identifying those costs can shed light on the evolutionary pressures influencing partner choice and inbreeding avoidance.

MATERIALS & METHODS