Intracolony social structure
Based on genetic and mark–recapture data, we can conclude that Bechstein’s bat colonies are composed of several matrilines, which are strongly philopatric. Currently, however, it is unclear whether the existence of two very distinct mtDNA lineages in 16% of the observed colonies (with a bi-modal haplotype distribution) are the result of rare immigration events or mostly reflect the founding history of the respective colonies (i.e. multiple mtDNA lineages founded a colony). Nuclear genetic diversity is maintained through mating away from the maternity colonies (Kerth et al. 2003) leading to high levels of diversity and low relatedness.
Recently, a detailed analysis of the fission–fusion dynamics in two colonies revealed nonrandom individual roosting associations that could partially be explained by kinship, with closely related females roosting together preferentially (Kerth et al. 2011). Nevertheless, unrelated females also formed long-term social bonds, and the mtDNA haplotype of females did not explain the strength of their associations (Kerth et al. 2011). For comparison, in big brown bats (Eptesicus fuscus), the only other bat species with fission–fusion behaviour for which genetic data are available, related females do not roost preferentially together (Metheny et al. 2008b). Finally, in Bechstein’s bats neither age nor reproductive status affected the strength of roosting associations consistently, a finding that partially contrasts to previous results, where reproductive status had a stronger effect than genetic relatedness (Kerth & Konig 1999). The precise reason for this contrast is unknown. It may be related to differences in methodology and sample size of the two studies, or indicates some flexibility in the social organization of Bechstein’s bat colonies.
Intercolony social structure
Similar to within colony analyses, substantial mtDNA differentiation between colonies suggests strong natal philopatry in females, and low levels of nuclear genetic variation within regions suggest outbreeding at swarming sites. Additionally, only weak structuring was seen across Europe suggesting that male dispersal and mating at swarming sites is effective at maintaining genetic homogeneity over large ranges.
These findings are confirmed by the long-term field data of marked females. No immigration of individually marked females into foreign colonies was observed. It is important to note that five of the altogether nine marked colonies lived together in the same forest with at least one other marked colony within potential daily roost-switching distance (2.8 km). In the permanently monitored BS colony, however, two unmarked females appeared, whose mtDNA haplotypes did not fit to that of the BS females. Instead they matched the haplotypes present in the colony IB3 that lived within 1 km of BS. Both immigrants arrived as subadults and established themselves successfully, changing status of BS from a colony with a unimodal haplotype distribution to one with a bimodal distribution. There was no evidence that these immigrating females and their offspring were less associated within the colony’s social network than the original colony members (Kerth et al. 2011). Interestingly, BS females behaved aggressively in previous experiments when confronted with members of the colony UH, carrying haplotypes similar to those of the later immigrants (Kerth et al. 2002b).
Bechstein’s bat social system
Using the observational, genetic, and parasitic data available for Bechstein’s bat, as well as supporting evidence from other species, we can begin to hypothesize about the origins and evolution of their peculiar closed societies.
We start with the observation that temperate-zone bats are much less variable in their social organization and mating system than tropical bats (McCracken & Wilkinson 2000; Kerth 2008b). The fact that in almost all temperate-zone bats, the females form maternity colonies suggests that in order to raise young in colder climates, females are forced to aggregate for social thermoregulation. However, it does not explain why males are rarely part of these maternity colonies, and why females are usually philopatric in temperate-zone bats, leading, in extreme cases, to closed societies observed in Bechstein’s bats.
The absence of males from the colonies probably has a twofold explanation. First, as in other mammals that cannot directly defend females or the resources they require (Clutton-Brock 1989), males resort to a promiscuous mating system, such as temporary harems or lekking. As female bats are highly mobile in three dimensions, are able to store sperm for several months, and their colonies often show high fission–fusion dynamics, in many species it becomes impossible for males to monopolize females (McCracken & Wilkinson 2000). Consequently, cohabiting with female bats during and directly after parturition is unlikely to strongly increase reproductive output in temperate-zone bats. Nonetheless, this does not explain why males rarely join the females in the maternity colonies.
We propose that in many species incompatibility in thermoregulatory requirements exists between males and females, although alternative explanations are possible (Senior et al. 2005; Safi et al. 2007). While females only infrequently go into daily torpor during gestation and lactation in spring and early summer in order to facilitate the growth of their offspring, males only require such investment during spermatogenesis in late summer and autumn, at times when females frequently use torpor to save energy (Racey & Entwistle 2000; for Bechstein’s bat see Pretzlaff et al. 2010). In species that roost in large cavities such as underground sites or buildings, sexual segregation may be present on fine scale only, with males and females roosting separately but in proximity to each other (and together at times when energetic requirements are similar). This incompatibility in seasonal timing of daily torpor of the two sexes in combination with the inability of males to monopolize females within their colonies, could explain female-only maternity colonies in most temperate-zone bat species. Upon segregation, further partitioning of roosting and hunting grounds is sometimes seen in species where females occupy optimal habitat (Senior et al. 2005; Safi et al. 2007). However, it is unclear whether males are forced from the optimal habitat by females, altruistically move away for the benefit of their kin in the colony, or simply avoid competition with the females by dispersing to available suboptimal habitats that are sufficient to sustain the lower requirements of the males throughout the summer.
The mating system of bats
The absence of males from the maternity colonies produces a new challenge, as the sexes now have to find a way to meet for mating. In temperate-zone bats, effectively three types of mating systems are observed: local recruitment, seasonal harems, and lek-like aggregations. Local recruitment at colony sites is obviously by far the easiest method of finding a mate, as auditory, olfactory, and perhaps even visual cues would be effective methods at such short ranges. On the other hand, local recruitment of mates carries the risk of inbreeding, especially in spatially isolated colonies where the immigration of dispersing males from other colonies would be rare. Nonetheless, it has been shown that local males sire substantial percentages of offspring in some species (e.g. Myotis daubentoni, Senior et al. 2005), but not in Bechstein’s bats (Kerth & Morf 2004), and interestingly in both cases inbreeding is not found. In case of the seasonal formation of harems, a single male recruits multiple females who then mate and roost together during several days. Here again, the possibility for inbreeding is present if females are recruited locally, but this has apparently been avoided in many species, such as Nyctalus noctula, where recruitment takes place during or after a seasonal migration of the females (Petit et al. 2001). Finally, males and females may assemble in leks, where promiscuous mating can take place. Indeed, many of the bat species found in the temperate-zone, including Bechstein’s bats, have a lek-like system known as autumn swarming (e.g. Parsons et al. 2003; Kerth 2008b).
During swarming, many males and females assemble at potential hibernacula in the months prior to hibernation and mate promiscuously. How swarming sites are established and how juveniles localize them in their first year of life remains a mystery (Kerth 2008b). However, once established, bats should have no trouble returning to such traditional sites in subsequent years because of their good navigational abilities (Holland et al. 2006). During swarming in Bechstein’s bats, siring occurs primarily by unrelated males, as suggested by the almost complete lack of structure between colonies in nucDNA (Kerth et al. 2002a, 2003). Thus, despite living in closed societies, Bechstein’s bats avoid inbreeding through promiscuous and probably random mating at swarming sites away from their summer habitat where they meet with large numbers of unrelated males.
Causes for closed maternity colonies in Bechsteins’s bats
As mentioned in the introduction, dispersal barriers cannot be the reason why colonies are closed, due to their close proximity and the bats’ ability to fly. Indeed, solitary males regularly disperse between the home ranges of different colonies (Kerth et al. 2000; Kerth & Morf 2004). Other explanations such as the defence of local resources, although a common reason for intercolony female competition in many other species (Stockley & Bro-Jørgensen 2011), also do not appear to apply in the case of Bechstein’s bats. Foraging grounds of females sometimes overlap with those of other colonies (Kerth & Melber 2009), and do so regularly with those of males (Kerth & Morf 2004). Indeed, it seems highly unlikely that the females could defend individual foraging ranges that are known to cover several hectares of forest. Exclusion to protect the microclimate of the roosts is also an implausible benefit, as more bats in a roost would provide energetic benefits for all females during pregnancy and lactation (Pretzlaff et al. 2010). Indeed, maternity colonies appear to provide an egalitarian environment. None of the typical types of intra-group female competition, as reviewed by Stockley & Bro-Jørgensen (2011), ranging from open aggression to more subtle forms such as reproductive inhibition have not been observed within Bechstein’s bat colonies. Nevertheless, the observation that colony members do not allow immigrants to join during confrontation tests (Kerth et al. 2002b), suggests that the pressure against the immigration of foreign bats is strong.
A possible explanation for xenophobic behaviour and the evolution of closed societies are fitness benefits from cooperation with close kin. In Bechstein’s bats, a strong influence of kin selection on the evolution of closed societies however seems unlikely for several reasons. For one, common cooperative behaviours such as allogrooming and information transfer among roosts are not restricted to close kin (Kerth & Reckardt 2003; Kerth 2008b). Furthermore, as social network analysis has shown, individualized roosting associations occur between unrelated females as well as related females, suggesting it is not essential for individuals to be related for social relationships to be established (Kerth et al. 2011). Moreover, the promiscuous mating system combined with the birth of maximally one offspring per female per year mean that genetic relatedness dilutes quickly within colonies (Kerth et al. 2002b). This can be seen by the high within-colony diversity and low differentiation between colonies in nucDNA. Nevertheless, colonies may be closed because of benefits arising from cooperation with familiar individuals. It remains to be tested, whether female Bechstein’s bats indeed benefit from living together with familiar colony members.
The argument that females do not switch colonies because of familiarity with the habitat cannot be fully excluded but seems unlikely to be the crucial selective pressure towards the evolution of closed societies in Bechstein’s bats. Females are faithful to individual foraging areas over many years (Kerth & Melber 2009), suggesting that long-term information about profitable foraging sites could be important. However, dispersing males are able to establish new foraging areas (Kerth & Morf 2004) and there seems no reason why females should not also be able to do so if dispersal becomes beneficial. Within colonies, information about roosts is shared among members through leading and following each other to roosts in combination with calling and swarming at roost entrances (Kerth & Reckardt 2003; Schöner et al. 2010). Theoretically, potential immigrants could exploit this way of information transfer and gain knowledge of roosts relatively easily, if only the local females would accept them in their roosts.
Finally, a plausible explanation for closed societies in Bechstein’s bats is parasite pressure. Bechstein’s bats have seemingly minimized contact with foreign conspecifics throughout their annual cycle. For example, mating at swarming sites produces high levels of outbreeding while minimizing body contact with conspecifics when compared to the mating harems seen in several temperate-zone bats, where bats from different colonies roost together for some days (Dietz et al. 2007). Also, Bechstein’s bats are generally observed to hibernate solitarily in rock crevices, or rarely, in small clusters of a few individuals, again more isolated from each other than observed in many other bat species (Dietz et al. 2007). While female Bechstein’s bats cannot completely avoid body contact with noncolony members during mating, in keeping their maternity colonies closed during summer, they effectively minimize any possibility for parasites to enter.
There are several reasons why parasite avoidance may be especially relevant in the case of bats. Most notably, bats harbour a large diversity of highly specialized parasites, bacteria, and viruses (Allen 1962; Calisher et al. 2006). This is likely due to the favourable conditions in maternity colonies, where parasites are provided with warm, immuno-compromised, and clustered hosts for them to exploit (Lourenço & Palmeirim 2008). The frequent roost switching of Bechstein’s bats and other bats has been interpreted as avoidance of parasites that deposit their larval stages in the roosts, such as bat flies (Lewis 1995; Reckardt & Kerth 2006). But roost switching does not help against contact transmitted parasites, such as wing mites, that only leave their individual hosts to move to another bat (Reckardt & Kerth 2009). For such parasites, transmission between colonies can be limited by living in closed societies, along with minimizing contact with noncolony members during mating and hibernation. Although the fitness consequences of wing-mites and other common ecto-parasites are generally considered to be minor (Giorgi et al. 2004; Lourenço & Palmeirim 2007), they may act as vectors and models for more costly endo-parasites, bacteria, viruses and fungi. A poignant example, which illustrates the effect that contact and/or close proximity with foreign bats can have, is the current spread of a pathogenic fungus (Geomyces destructans) causing the ‘White Nose Syndrome’ in North-American bats (Blehert et al. 2009). This fungus has wiped out up to 90% of the members of certain bat populations, affecting many colonies at the same time. Although living in closed societies during summer cannot completely protect against rapidly advancing infectious diseases such as G. destructans, it does have the potential to minimize parasites and pathogens transmission.
In addition to avoiding initial infection, prevention of local parasite adaptation may also be necessary (Gandon & Michalakis 2002). From the investigation of the genetic structure of the ecto-parasitic wing-mite of Bechstein’s bats (Bruyndonckx et al. 2009; J. van Schaik et al. in Prep.), we suppose that the bats successfully prevent this adaptation by limiting their colony size and keeping colonies isolated from each other during summer as well as by minimizing transmission though the mating and hibernation phase. Thereby the bats are causing strong genetic drift in the mites, which eliminates opportunities for local adaptation in the parasites (J. van Schaik et al. in Prep.).
To summarize, no single explanation can currently explain the existence of closed societies in Bechstein’s bats. The conclusion most consistent with the current data is that Bechstein’s bats benefit from living in closed societies because stable groups may facilitate cooperation and to reduce parasite pressure. We must however underscore that despite the large amount of knowledge gained about this system during the last 15 years, there remain several critical and untested assumptions in the explanation presented above. This includes possible benefits of stable long-term relationships among colony members as well as fitness consequences of infestation with different parasites. Also, it remains to be identified whether the rare acceptance of immigrants is an active choice (behavioural plasticity in response to critically low population size), or simply due to a lack of recognition among some colonies. Perhaps the largest gaps in our knowledge are details concerning the social interactions outside of the maternity colony. Swarming dynamics as well as potential hibernation associations have yet to be studied in detail, and could significantly contribute to the understanding of this interesting social system.
Consequences of living in a closed society
Living in a closed society has several positive as well as negative consequences. We already discussed the potentially positive influence on the evolution of cooperation, either through reciprocity among long-term associates, or through shared genes (kin-selection), and even by-product mutualism may be favoured in closed societies (Clutton-Brock 2002; West et al. 2002; Sachs et al. 2004). Interestingly, it has been shown that cooperation (in bacteria) is favoured via the budding dispersal of colonies as this maintains high relatedness, while reducing local competition (Kummerli et al. 2009). Thus possibly the budding of colonies as observed in big brown bats (Metheny et al. 2008a), and supposed for Bechstein’s bats, is not only a product of living in closed societies, but may also strengthen their advantage by increasing within colony relatedness and subsequently cooperation (Kerth 2008a). At the same time, living in closed societies may substantially limit the dispersal capabilities and genetic resilience of the species. For example, expansion and dispersal is only possible in the event that societies reach the critical size for allowing them to fission permanently. Also, rescue effects, where critically low population sizes in individual societies are prevented through immigration from other societies, are highly unlikely. This means that not only may the species have difficulties expanding its range, but it will also have difficulties maintaining declining populations. Finally, limiting dispersal to one sex may be risky, especially at the fringe of the distribution, or in the case of low population densities, due to the difficulty of locating individuals of the opposite sex outside of the natal society.
Comparison with other species living in closed societies
Unlike in bats and few other mammals, closed societies seem often to be connected with high reproductive skews among group members (a single breeding pair; Kerth et al. 2000). For example, the structure of eusocial insect colonies shows many parallels to those of the closed societies seen in cooperatively breeding mammals (Boomsma 2009). Whether due to direct kin selection (Helanterä & Bargum 2007) or multi-level selection (Wilson & Wilson 2007), it is clear that natal philopatry and demographic isolation is critical to the success of the colonies in eusocial insects. In mammals, a similar example can be found in two mole rat species, which live eusocially in large colonies with highly related males and females. Here, not only cooperation among kin but also ecological constraints such as restrictions in food availability and the high costs of dispersal are hypothesized to be the reasons for the (almost) strict natal philopatry of both sexes and the evolution of closed societies (Burda et al. 2000). Nonetheless, even in naked mole rats substantial outbreeding and occasional dispersal of males is observed in the wild (Braude 2000) and negative effects of inbreeding have been documented following the outbreak of a novel disease in the lab (Ross-Gillespie et al. 2007).
Some other mammals show closed societies without strong reproductive skew (having multiple breeders). One example is the killer whale (Orcinus orca), which forms philopatric pods of males and females, and mating only takes place during temporary interactions with other pods (Pilot et al. 2010). In this species, a strong limitation to dispersal is provided by clear foraging specializations (ecotypes) (Dahlheim et al. 2008). As learning of such specializations requires a large individual investment, it is supposed that individuals do not disperse to pods specialized in other foraging strategies. Surprisingly, dispersal between pods within ecotypes is also rare, and cannot be explained as a function of either cooperation or dispersal barriers so far (Pilot et al. 2010).
Outside of bats, perhaps the most similar society to those of Bechstein’ bats is that of the white-nosed coati (Carnivora: Nasua narica). In this species females are philopatric (Gompper et al. 1997), and males only join female bands during brief mating periods (Booth-Binczik et al. 2004). Males disperse from their natal bands, probably to reduce resource competition (Gompper et al. 1998), and female bands are only formed via fissioning of existing bands. Nonetheless, dispersal of females away from their natal bands does occur, and seems to be most successful when done together with a partner (Russell 1983; Gompper et al. 1997). Social behaviours such as allogrooming are observed (Gompper 1997) and female bands also maintain and defend well-defined home ranges. Therefore, it seems likely that cooperation among kin (and potentially long-term band-mates) acts as the driving force leading to extensive natal philopatry and almost closed bands in coatis.
Finally, although a large variety of female-bonded societies can be observed in primates (Kappeler & van Schaik 2002), virtually all primate societies comprise males and females, and usually at least one sex is able to regularly disperse between societies. Hence, to our knowledge no examples can be shown where societies of primates are as closed as in Bechstein’s bats.
In conclusion, the closed female societies observed in Bechstein’s bat (and potentially several other bat species) appears to be unique within the mammals. This suggests that the pressures selecting for this unusual social system may be relatively specific to bats, yet at this point no definitive cause can be identified. Knowledge of the causes for closed female societies however may be highly relevant towards understanding the factors shaping the evolution of mammalian societies. Unfortunately, the long term data sets required for detailed characterization of social systems, especially in combination with analysis of additional pressures such as parasitism are still rare, making comparative studies unfeasible at this point.
Studying closed societies: an evaluation of the available methods
As we have shown, a large amount of detailed knowledge is required to adequately characterize and hypothesize about the causes and consequences of the social system of a species. With respect to field data, it is especially important to observe social interactions that cannot be investigated genetically because they do not result in gene flow. This includes occasional visits between social groups and individual roosting associations as well as behavioural mechanisms, such as xenophobic behaviour, that keep societies closed. Moreover, field data may provide an independent measure for dispersal rates and distances as well as estimates of individual fitness parameters. Hence field data shed light on the benefits and costs of living in particular social organizations that genetic data alone cannot fully address.
Regarding genetic approaches, it is evident that selecting the suitable genetic markers and techniques is critical. It has long been known that the analysis of mtDNA and nucDNA will shed light on different parts of the social system of a species, but we would like to emphasize that this is in particularly the case for species with extreme sex-specific dispersal rates such as Bechstein’s bats. As a number of reviews and comparisons have illustrated (de Meeus et al. 2007; Meirmans & Hedrick 2011; Wilkinson et al. 2011), the last decade has seen remarkable advances in the analysis of population genetic data. Consequently, it is becoming increasingly important to carefully select the proper analytical tools (Excoffier & Heckel 2006). In our study, use of any of the measures for analysing nucDNA (FST, G″ST, DST, Assignment tests, amovas) have resulted in similar conclusions, making it difficult to decide which measure agreed best with the field data. However, it must be emphasized that none of the measures used is optimal for all types of studies (e.g. dispersal, drift, demography, within/between population; Meirmans & Hedrick 2011).
As a final note, it is important to not only consider the species at hand, but also those interacting with it. Parasites, while often ignored, can offer extra insights into the interactions of a species with conspecifics and their environment (Nieberding & Olivieri 2007). Likewise, apart from observational and genetic data, which must be gathered on the species in question, comparison with related species can be a powerful tool. Often species within a genus/order show variations in social system, and contrasting such variations can give insight into the selection pressures that caused them.