Monogamy within the Termite World: Mate Choice and Colonial Structure

Becca Knox Term Paper 4/10/2013 Monogamy within the Termite World: Mate Choice and Colonial Structure Abstract Serial monogamy found in social insects, as a contrast to the promiscuity displayed by many organisms, contributes to profound advantages within a colony. For termites, mate choices often occur before copulation; the colony is first founded and the nest is secured before sexual reproduction transpires. In addition, the lifetime pairings are formed early in life. Bonds of this type are as strong of a commitment as the joining of two cells to create a zygote it is an extreme sense of commitment. Most often found in eusocial insects, the reproductive division of labor from sterile castes, and decreased mating variation as a result of this monogamy imply that lifetime commitment is a major factor in contributing to higher levels of organization within colonies. In addition, the lack of conflict over parental dominance has led to more harmonious relationships between offspring and parents. From an evolutionary standpoint, eusociality and monogamy may have stemmed from such characteristics as the overlap of generations, the advantages of group defense and colony structure, as well as the possibility to inherit the nest by offspring. The factors involved with mate choice and colony structure vary between different monogamous insects. However, recent studies on the mating biology of eusocial living have shown that termites make fascinating study species to decipher the relationship between eusociality and monogamous systems of mating. In fact, researchers have shown that even after long separations from colonies, termites are still able to recognize their colony mates. Though some antagonistic behavior was displayed, no mortality ensued. Cooperation among termites from the same colony are ways in which the species ensure that ecological competition and pressure does not promote internal aggression (Korb and Foster 2010). Kin recognition among

termites may be influenced by cues that are encoded genetically such as chemical olfactory cues, as well as differences in greeting behavior. These aspects of recognition raise interesting questions about how lifetime mates are chosen and how recognition of the mate becomes established. Introduction Eusociality and monogamy are often closely associated with one another within the insect world. Multiple theories about the evolutionary relationship between lifetime partnership and eusociality are important areas of study, especially as the benefits of monogamy and kin selection come to the forefront. There are several hypotheses for the evolution of this monogamous structure in termites, many of which emphasize the role of the male as crucial to the colony in terms of defense and sperm production (Nalepa and Jones, 1990). The biology of termite queens and kings as well as the establishment of different castes are fundamental aspects of the way the colony functions and becomes successful. The system of haplodiploidy and kin selection are also factors involved with the evolution of monogamy and eusociality, which contribute to the stability of a termite colony (Fromhage and Kokko, 2011). The benefits of monogamy for eusocial insects are multitudinous and include amicable cooperation among offspring and parents where conflict would lead to their demise, possible nest inheritance, and promotion of stability within the colony (Gadau and Fewell 2009). Researchers have discovered that termites make for intriguing study species to explore the relationship between eusociality and monogamous behavior, especially since mate choice is not random, but rather carefully selected before copulation occurs. In addition, termites are the second largest animal taxon to express monogamous behavior in which both parents are involved with the care Knox, 2

of the colony; termites are therefore a crucial component of serial monogamy research (Shellman-Reeve 1999). Though this model of monogamy does not apply to all species of termites, nor all insects that have evolved eusocially, the differences in mating patterns among other termite species and eusocial hymenoptera make for exciting opportunities for study and comparison. In many cases, the polyandry discovered within other colonies emphasizes the peaceful interactions and other advantages found within monogamous super organisms. Mate Choice and the Advantages of Monogamy Because the commitment of termite queens and kings is so substantial, they choose their partner fastidiously. Evidence for non-random mating has been discovered within populations of Coptotermes lacteus in which the different colonies were significantly deficient in heterozygotes, indicating that mate choice was selective (Thompson et al. 2006). However, it is difficult to tell whether the inbreeding of these termites resulted from ecological constraints or actual genetic preferences (Thompson et al. 2006). Females and males use different physiological characteristics of the other in order to make a mate choice. For instance, females often use large head size variance as a determinate of mate pairing, while males focus on fat and body mass when making a choice (Shellman-Reeve 1999). This investment made within a partnership choice stems from the intensity of the commitment as well as works as a way to determine and secure the quality of the mate choice. In a recent study, termites that had previously been rejected as a mate choice were more likely to end up with a partner that had also been rejected (Shellman- Reeve 1999). In this way, termites with smaller heads often paired with females of smaller body mass. These differences within the criteria used by each gender may be explained by the Knox, 3

indicators of each characteristic. Head width, for instance, displays whether a male can defend a nest and would be a good protector, and female body mass may be an indicator of future fertility (Shellman-Reeve 1999). Once making a mate choice, both partners are heavily involved with the construction and establishment of the colony, including involvement with care of the young, which suggests the extensive investment made by each committed partner (Shellman-Reeve 1999). It is interesting to note that mate choice occurs before consummation of the relationship which places more pressure upon the physical attributes of individuals as determinants for partners (Boomsma 2013). There are a myriad of advantages to monogamous behavior, not least of all, the harmonious cooperation of individuals which results from the lack of conflicts involving parental commitment (Boomsma 2013). Within a eusocial society, the mother conducts care of the young in cooperation with the labor performed by sterile castes. These established roles promote harmonious interactions because there is no uncertainty or conflict over behavioral roles (Boomsma 2013). In fact, these roles are often irreversible, and established early in life (Hartke and Baer 2011). Another advantage of monogamy includes the potential for a worker s ability to inherit the nest (Gadau and Fewell 2009). Because some workers still maintain their reproductive capabilities, they are able to take over the colony in the event of the death of the king and queen. For instance, in the species Reticulitermes virginicus, kings and queens may be succeeded by juveniles when sexually mature. When the king and queen decease, as opposed to being fatal for the colony, in this species, the neotenics of the colony replace the king and queen. The neotenics are developed as a result of not having access to a male. Some of the colonies of this species consist of parthenogenetic females, or those which have the ability to reproduce without Knox, 4

fertilization (Vargo et al. 2012).The death of the king and queen makes way for the development of neotenics, which therefore establishes the advantages of staying within the nest (Gadau and Fewell 2009). The nest, and the role of reproductive can be inherited. Additionally, advantages of group living within a monogamous colony include the safety provided by the nest itself. The risks of leaving and establishing a new colony are tremendous, and thus also influence the termite worker s desire to stay with the nest (Gadau and Fewell 2009). Though a few species of termites have the ability to develop replacement reproductives, the loss of the queen and king within a colony can be detrimental to the nest. A main reproductive pair is crucial to the long-term sustainability of the colony. A recent study shows that the survival rate of the colony is vastly superior while a colony maintains its king and queen reproductives opposed to more negative results that occur from worker developed reproductives. This biparental method of care and establishment of the colony, therefore, is vital to the health, efficiency, and stability of the nest (Hartke and Baer 2011). Mating Biology of Termites and Caste Determination In termites, the males are able to be long-lived, similar to the queens, and produce a continual supply of sperm, often for up to a couple decades at a time (Hartke and Baer 2011). In contrast to more promiscuous species, the sperm cannot be tested by the female before mating occurs. Rather, mate choice comes after the nuptial flights, and before copulation. In this way, the termite king as a sperm producer is a key concern to females (Boomsma 2013). Despite the continual presence of the king termite, the queen also stores sperm within the spermathecae. This behavior suggests that minimalization of sperm loss or waste is lessened by the storage structure (Boomsma 2013). The size of the colony is determined by the amount of Knox, 5

eggs the queen is able to fertilize and produce. In addition, neither the female nor the male have external genitalia, pointing to the idea that sexual selection pressures are not key factors in their evolutionary development (Hartke and Baer 2011). What is termed a royal pheromone is a substance which impedes the reproductive behavior of worker castes. Though the chemical compounds are unknown, the presence of the compounds corresponds with a reproductive s status and age, which therefore regulates the termite caste system (Hanus et al. 2010). It should not be said that termite workers are helpless dupes which suffer under the repressive reign of a king and queen. In reality, recent studies have shown that cuticular hydrocarbons act as important chemicals in insect communication and workers are decision-making individuals involved with reproductive potency coordination and modifications made within the caste system (Hanus et al. 2010). Another factor involved with caste regulation includes the differentiation of termite soldiers. The caste of a particular termite is not determined from an individual basis, but rather stems from the termite queen and king stimulation. When the primary reproductives were removed from the colony, no soldiers were developed, suggesting the necessity of the king and queen. Soldiers were seen to develop when given more proctodeal, or anus-to-mouth, feeding materials than other third instar larvae (Maekawa et al. 2012). An increased level of JH is also needed to promote the development of soldier termites, which is thought to be procured through additional proctodeal methods. For insect worker castes other than soldiers, it has been suggested that sterile castes within eusocial insect groups necessarily arose from the monogamous behavior of the parents, which then points to the idea of worker altruism and kin selection (Boomsma 2009). Knox, 6

Termite Worker Altruism and Kin Selection Eusocial colonies rely upon sibling behavior which consists of altruistically helping raise siblings rather than reproducing themselves (Hughes et al. 2008). These sterile individuals help take care of their siblings at the cost of personal reproduction of their own progeny (Boomsma 2009). This kin selection strategy of termites that care for their siblings rather than their own offspring, often at the possible cost of their own survival, comes from the amount of relatedness that each sibling shares with one another. This similarity continues through genes, and so the survival of offspring necessarily also coincides with the survival of similar genes, albeit within a sibling rather than offspring. Additionally, termite workers benefit from their altruistic behavior through protection and sustenance. The assistance of brood care of siblings can be viewed as a sort of surrogate, or replacement for the worker s own offspring (Boomsma 2009). Because of this relatedness of siblings, termite workers have been shown to recognize kin mates even after long periods of separation. When termites were paired with those from a different colony, significant mortality and aggression ensued; in contrast, termites paired with those they had been merely separated from but were of the same colony, featured mild levels of offensive behavior and no mortality (Olugbemi 2012). The ability to recognize mates is suggested to come from similarities of olfactory cues which may have been genetically encrypted, as well as similar receptors and greeting behavior (Olugbemi 2012). Rather than initiating a battle between related termites that had been separated for a long period, these termites were shown to begin building tunnels together. Relatedness of siblings therefore is a key element to the importance of kin recognition as well as harmonious cooperation among individuals and the promotion of altruism. Knox, 7

Though altruistic behavior was previously thought to have been a cause of the evolution of eusocial living, recent research shows that the behavior is actually an effect of eusociality (Hughes et al. 2008). For instance, group living is safer and has a higher survival rate than it would be for a solitary termite. Thus, though a termite colony may be composed entirely of kin, this relatedness is a result of eusociality and is beneficial toward individual workers. This can be contrasted to polyandry activity in which the offspring is increasingly less related if there are multiple breeding females within a colony (Hughes et al. 2008). A high level of relatedness among workers is an essential factor in concordant eusocial living. Evolution of Monogamy in Connection with Eusociality There are many characteristics that are involved with the evolution of eusociality including the overlap of generations, monogamy, and the benefits of group defense and protection. Individuals who help within the colony provide it with a higher probability of survival, which is beneficial to all. Eusociality may have also been derived from the ability of some workers to maintain their reproductive capabilities and thus promote the adaptation and development of a colony (Thorne 1997). A definitive conclusion about the evolution of eusociality and monogamy is impractical, but many hypotheses combine to contribute to a more complete understanding of these questions. For example, advanced eusocial insects are predominantly monogamous, which suggests that the evolution of the division of labor with sterile workers came from lifetime monogamy (Boomsma 2007). The two concepts appear indissolubly linked. Though there are multiple hypotheses for the derived nature of termite monogamy, one hypothesis states that in order to have a lifetime supply of sperm production, the continual presence of a male is needed, and another is the idea of mate guarding (Nalepa and Jones 1990). Knox, 8

A third hypothesis incorporates both hypotheses as well as emphasizes that ecological constraints contributed to this evolutionary phenomenon as well. The first hypothesis involving sperm production was derived from the understanding that queen termites are extremely fertile, and long lived. Therefore, without the presence of a male, the female would have to have a complex sperm storage area that would keep the sperm useful even after long periods of time which is not the case (Nalepa and Jones 1990). Additionally, within the second hypothesis, the limited availability of females at the same time as all the other females forces males to make a choice directly after the nuptial flights, and this mate guarding leads to the monogamous result. The male termite s success rate at reproduction is improved by its continual engagement with one female individual, especially since the energy and time spent finding a mate is so costly (Nalepa and Jones 1990). However, the ecological limitations of sparse food resources, the difficulties involved with being a lone termite without a colony, and the difficulty of finding a mate should also be taken into account when the evolution of monogamy is concerned (Nalepa and Jones 1990). In addition to monogamous behavior, haplodiploidy is also a factor often connected with the evolution of eusocial insects because it increases the probability for eusocial behavior to develop and become stable (Fromhage and Kokko 2011). Species that are haplodiploidy, are thought to be more conditioned to the system of eusociality because the individuals are more closely related than to their would-be offspring (Fromhage and Kokko 2011). However, a recent study furthers the importance placed upon this haplodiploid system. The study shows that the expected percentage of termite sisters that have a rare phenotype is larger in haplodiploid than in diplodipoid, suggesting that the stability of a eusocial colony relies upon haplodiploidy to guard Knox, 9

against rare individual alleles (Fromhage and Kokko 2011). Monogamy as well as haplodiploidy are both crucial factors for the evolution of eusociality. Polyandry within Eusocial Insect Groups As a contrast to the stability promoted within a colony by monogamy, promiscuous behavior adversely affects the benefits otherwise gained from parental commitment and kin altruism (Boomsma 2007). Because females mate multiple times, the relatedness of individuals to one another is decreased, and sexual competition over paternity is increased (Jaffe et al. 2012). However, some promiscuity in other eusocial insects seems to have some beneficial effects. Though the honey bee queen is promiscuous, this behavior seems to promote worker productivity as well as allows workers to shift their own fertility as the mating rate of the queen decreases. When the queen bee is only inseminated by one male, workers selfishly take resources from the colony to promote their own reproductive capabilities. In this way, the mating activity of honey bee queens influences the reproductive response of workers to alter the movements of individuals and results in reduced activity and performance (Mattila et al. 2012). Inversely to the monogamy found in most termites, as the honey bee colony workers become more closely related from a decrease in queen polyandry, reproductively active honey bee workers are often met with hostility by other workers. Promiscuous activity by the queen therefore establishes more peaceful cooperation among individuals (Mattila et al. 2012). Similarly, the males of the hymenopteran species Ropalidia marginata also engage in promiscuous behavior, but females do not (Shilpa et al. 2010). The male wasp of this species mates multiple times in order to secure that its sperm continues, however, the female wasp is reluctant to mate multiple times which a recent study notes contributes to increasing the harmony Knox, 10

of more related individuals within the colony (Shilpa et al. 2010). The idea of monogamy as enhancing cooperation among colony members coincides with the monogamy found within most monogamous termites; however, it is interesting that there is a discrepancy between the level of commitment of the female wasps versus the males (Shilpa et al. 2010). It is fascinating to note that the eusociality of bees, wasps, and termites evolved separately from one another, and yet are somewhat similar in terms of mating patterns (Boomsma 2013). Conclusion This review reveals that though there are exceptions to the evolutionary link typically made between monogamy and eusociality, the benefits of monogamous behavior within the superorganism are multitudinous. In termites as well as eusocial hymenoptera, mate-choice is made outside of the colony the event occurs after the reproductives have left their natal nest and search for their own partners, rather than being a part of societal living (Boomsma 2013). The monogamy of the primary reproductives in termites has been shown to create a more harmonious and stable living environment for their offspring, especially since kin selection is a key aspect of fostering this stability. Further research needs to be done in terms of the chemicals found within the royal pheromone to enhance understanding about caste determination of soldiers, as well as the evolutionary relationships among eusocial insect groups. Termites and the development of lifetime partnerships provide incredible insights into the benefits of monogamous behavior, especially as it relates to worker altruism and the cooperation among termite workers which decrease internal conflicts. Knox, 11

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