Study of Dunnock Mating, The
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KeywordsBehavioral Ecology Sexual Conflict Mating Combination Monogamous Pair Polyandrous Female
The study of natural history, behavioral ecology, and evolution of dunnocks, Prunella modularis, with respect to their intriguing mating behaviors.
A mating system is a description of the processes by which males and females acquire mates. Mating systems are generally stable within and among populations of a species. For instance, most avian species could be described as socially monogamous, meaning that males and females form pairs during the breeding season to mate and, occasionally, to raise young together. Within this typical bird population, most individuals would breed as pairs.
At least since the 1950s (Campbell 1952), bird watchers and researchers suspected that a little dull brown bird, the dunnock, Prunella modularis, would hold some surprises about their mating behaviors. But it was not until the 1980s that studies using color-banded individuals (i.e., marked with a unique combination of colored plastic rings on their legs) provided insights about the curious mating behaviors of dunnocks. These studies (Birkhead 1981; Karanja 1982) confirmed what was suspected since at least the 1950s; dunnocks presented considerable variation in mating combinations. Far from the usual monogamous bird species, dunnocks presented within-population variation in mating patterns. Dunnocks breed as pairs (monogamy), groups of a male with two females (polygyny), a female with two or more males (polyandry), or even groups of two or more males sharing several females (polygynandry) (see Davies 1992). Such within-population variation in mating patterns is unique across animals, making the dunnock an interesting study system for understanding the evolution of mating systems.
Dunnocks are also known for a peculiar sexual behavior, first described in 1902 by the ornithologist Edmund Selous. The behavior – named cloaca pecking – is part of the precopulation display performed before a copulation attempt. During this display, the male hops around behind the female while she shudders her wings and raises her tail to expose her cloaca (see Davies (1992) for a thorough description). The male will then peck at the female’s cloaca several times within a minute before he copulates with her. Occasionally, the female will dip her abdomen and eject a droplet of sperm. Males only copulate after females eject this droplet. Nick Davies (see Davies 1992) interprets the behavior as a female attempt to convince the male that he has a chance of gaining paternity. Consequently, encouraging him to stay with the female and provide care toward her young. Davies’ interpretation makes sense because social polyandry is a common mating strategy in dunnocks. That is, in social polyandry, females are simultaneously paired with two or more males that copulate with her.
Once these naturalistic studies identified that dunnocks possessed a variable mating system – that is, one in which there was variation in the mating compositions – the focus shifted toward hypothesis-driven studies based on theory. Davies, who was one of the founders of the field of Behavioral Ecology, employed evolutionary theory to investigating the variable mating system of dunnocks (see Davies 1992). The long-term study by Davies in England has helped us to understand many aspects concerning dunnock mating behavior and contributed to the field of behavioral ecology in general. For instance, Davies’ study provided understanding of parental investment and sexual conflict theories (see the section “Cross-References”). Davies’ studies have become a textbook example of mating systems. More recently, another study – using an introduced population in New Zealand (see Santos (2012) for details about the introduction history of dunnocks) – has also investigated the mating system of dunnocks to address behavioral and evolutionary questions. These recent studies have found several new facts and unexpected insights into dunnock mating behavior (see below).
Variable Mating System
The Cambridge (see Davies 1992 for details) and the Dunedin (Santos et al. 2015 and references therein) studies provide information on the formation of the different mating types. Apparently, the mating combinations are a consequence of variation in male and female territory size, and competitive ability of individual birds. Unlike other birds, female dunnocks do not choose males based on their territories or territorial attributes. Females appear to choose their breeding territories independently of males, and female settlement is based on competition with other females for space. Thus, a mating combination – for instance, monogamy – is the result of a small female territory and a male with enough competitive ability to ward of male intruders. Social polyandry is likely to result from a large female territory that overlaps with at least the territories of two males. These males, in turn, chase the female around her territory, while fighting with each other. These male-male interactions result in a dominance hierarchy, and then these males coalesce their territories.
In the Cambridge study, territory size was different between polyandry (0.71 hectares) and monogamy (0.28 hectares). Meanwhile, in the Dunedin study, polyandrous and monogamous groups had similar-sized territories (0.24 hectares) (Santos and Nakagawa 2013). Thus, it seems that while in Cambridge female territory size is an important characteristic shaping the variable mating system, in Dunedin it seems that female territory size may play a smaller role.
Both studied populations presented male-biased adult sex ratios, that is, there were more adult males alive during the breeding season than adult females. In Cambridge, males represented 54.5% of adults, while in Dunedin males represented 57% of breeding adults. Compared to the Cambridge and four other dunnock studies (Davies 1992), the Dunedin population had the highest density of males per hectare, averaging 5 males/hectare, while the Cambridge population averaged 2.6 males/hectare. These demographic differences are probably associated with differences in the frequency of the within-population mating combinations. For instance, in Dunedin – with high male density and skewed sex ratio – territories are small, and social monogamy and polyandry are the predominant mating combinations.
In evolutionary terms, the different mating combinations yield different fitness payoffs to males and females. In species like the dunnock, in which males feed the nestlings, the fitness consequences of the mating combinations are important to breeding individuals. From a fitness perspective, polyandry is the optimal breeding situation for females because multiple males provide care. Yet from a male perspective, sharing the same female with another male is not optimal. Theoretically, this occurs because a male may lose paternity to his co-breeding male partner. Dunnock mating systems, therefore, are an example of sexual conflict. The development of genetic analyses allowed for the investigation of maternity, paternity, and relatedness between individuals, yielding insights into the consequences of the sexual conflict in dunnocks.
The Genetic Eyepiece
In 1989, Burke and collaborators (Burke et al. 1989) applied a technique called DNA fingerprinting to dunnocks from Cambridge to investigate the relationship between the mating behavior of birds from the different mating combinations and genetic paternity. In social monogamy, all chicks were sired by the resident male. In the polyandrous groups, in which the male hierarchy dictates mating access to females, the dominant and subordinate males split the paternity of broods almost evenly. These findings showed that even with little mating access to the female, subordinate males could gain paternity in polyandrous groups.
Santos and colleagues (Santos et al. 2015) also investigated how paternity was distributed among dunnock broods in Dunedin. In this study, the authors used microsatellite markers to generate individual genetic profiles used to assess paternity and relatedness among dunnocks. The Dunedin study revealed differences in the genetic mating system of dunnocks. While in Cambridge there was little evidence of extra-pair or extra-group paternity – offspring that were sired by males other than the males from the social breeding group – in Dunedin, extra-pair and extra-group paternity was abundant. Extra-group paternity occurred both in socially monogamous and socially polyandrous groups. Over 30% of broods from socially monogamous pairs had at least one chick that was sired by an extra-pair male, while 17% of broods from socially polyandrous groups had at least one extra-group young (Santos et al. 2015). These data suggest that (i) males in socially monogamous pairs are not as efficient in guarding their mates against intruders as two or more males in socially polyandrous groups; and (ii) females in socially monogamous pairs have more opportunities to leave their territories and engage in extra-pair copulations than socially polyandrous females.
The paternity data from the Dunedin study also changed how we interpreted the reproductive payoffs from a male perspective. Davies and collaborators showed that males had highest reproductive success with polygyny, less with monogamy, and least with polyandry (summarized in Davies 1992). This is the theoretical expectation when males do not lose paternity to extra-pair males. However, in Dunedin, extra-pair or extra-group paternity accounts for the paternity of 23% of young in social monogamy and 10% of young in social polyandry. Considering all the paternity lost and gained by including extra-pair or extra-group paternity in the estimates, Santos and collaborators (2015) showed that the number of young fledged per breeding attempt was similar among three types of males: socially monogamous, alpha, and beta co-breeding males. Thus, from a male perspective, sharing a female with another male in a socially polyandrous group is not such a bad reproductive tactic.
Moreover, the Dunedin study has also showed that when females engage in multiple mating that leads to mixed-paternity clutches, they avoid negative effects caused by inbreeding. Additionally, an increase in the relatedness between breeding males and females in social monogamy decreases hatching success of the eggs. The relatedness between individuals had another biologically relevant consequence. Many male coalitions in polyandrous groups were closely related in Dunedin; that is, their relatedness estimates ranged from cousins to offspring/full-sibling. The consequence of breeding together for these closely related males is that they also gain indirect fitness benefits (estimated at approximately 5% of their direct reproductive success). In Cambridge, through detailed observations, Davies and colleagues did not observe any instance of closely related individuals breeding together.
Personality and Its Implication for Dunnock Mating
Another study in Dunedin has investigated the relationship between “personality” genes and behavior. Among other findings, Holtmann and collaborators (2016) found significant allele effects for the association between the mating status of a dunnock and its genotype at two “personality” genes. These genes are the serotonin transporter gene (SERT), for which allelic variation has been associated with several behavioral phenotypes in other species, and the dopamine D4 receptor gene (DRD4), in which variation is associated with exploratory behavior and activity in vertebrates. Mating status was defined as the individual’s social mating composition. This study classified individuals into four mating statuses: (i) monogamous females, (ii) monogamous males, (iii) polyandrous females, and (iv) co-breeding males. These categories represent the different degrees of promiscuity exhibited by individuals. Individual mating status was repeatable across three breeding seasons, meaning that birds were consistent with respect to their mating categories. The intra-class correlation (i.e., repeatability) of male mating status was on average of 73%, while female mating status had an intra-class correlation of 60%. Notably, males that were homozygous for two SERT alleles (namely SNP840 and SNP966, see Holtmann et al. 2016) were on average 27% more likely to form a coalition with a co-breeding male than heterozygous males at these alleles. Overall, these findings indicate that genomic information will become an increasingly important tool in the study of mating systems.
The study of dunnock mating started with curious naturalistic observations. When these naturalistic observations were acknowledged and studied in a systematic manner, dunnocks became a textbook example of a unique mating system and shed light on several important theoretical areas. It is through the combination of naturalistic observations, a theoretical foundation to stimulate study questions, and long-term studies that what could have been an anecdotal observation of a little brown bird became an essential asset in behavioral ecology and evolutionary biology.
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