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