Delayed dispersal as a potential route to cooperative breeding in ambrosia beetles

Xyleborini are a species-rich tribe of ambrosia beetles, which are haplodiploid and typically mate among siblings within their natal brood chamber. Several characteristics of this tribe would predict the evolution of higher levels of sociality: high genetic relatedness within galleries due to inbreeding, high costs of dispersal and the potential benefit of cooperation in brood care within the natal gallery (e.g. by fungus gardening, gallery extension, offspring feeding and cleaning). However, information on the social system of these beetles is very limited. We examined the potential for cooperative breeding in Xyleborinus saxeseni by monitoring dispersal in relation to brood size and composition. Results show that adult female offspring delay dispersal despite dispersal opportunities, and apparently some females never disperse. The females' decision to stay seems to depend on the presence of eggs and dependent siblings. We found no indication that female offspring reproduce in their natal gallery, as colonies with many mature daughters do not contain more eggs than those with few or no daughters. There is a significant positive relationship between the number of females present and the number of dependent siblings (but not eggs), which suggests that cooperative brood care of female offspring raises colony productivity by improving survival rates of immatures. Our results suggest that cooperative breeding is likely to occur in X. saxeseni and possibly other xyleborine species. We argue that a closer look at sociality within this tribe may yield important information on the factors determining the evolution of cooperative breeding and advanced social organizatio

The influence of social experience on cooperative behaviour of rats ( Rattus norvegicus ): direct vs generalised reciprocity

Cooperation among non-kin has been attributed sometimes to reciprocal altruism: Two or more individuals exchange behaviour that benefits the respective partner. According to direct reciprocity, cooperation is based on past behaviour of a known partner. In contrast, in generalised reciprocity, cooperation is based on anonymous social experience where the identity of the partner is irrelevant. In a previous study, female Norway rats (Rattus norvegicus) were found to cooperate according to a generalised reciprocity mechanism. In this study, we tested whether Norway rats would also cooperate as predicted by a direct reciprocity mechanism and whether direct reciprocity would cause a higher propensity to cooperate than generalised reciprocity. Focal animals were experimentally manipulated to receive social experience from known or unknown, helpful or defecting partners in an instrumental cooperative task. Our first experiment shows that rats are more helpful towards a partner from which they had received help before than towards a partner that had not helped (i.e. direct reciprocity). Our second experiment revealed that after receiving help by others, rats were more helpful towards a partner from which they had received help before than towards a new partner (i.e. direct reciprocity generated a higher cooperation propensity than generalised reciprocity). We conclude that in female Norway rats, the tendency to cooperate is influenced by partner-specific information. To our knowledge, this is the first study to demonstrate direct reciprocity in rodents, and it is the first study testing direct vs generalised reciprocity in animal

Female choice of a non-bodily ornament: an experimental study of cichlid sand craters in Cyathopharynx furcifer

In many species of East African cichlids, males build sand craters or "bowers” to attract females for spawning. It is commonly assumed that these exaggerated sexual traits have a function similar to bodily ornaments. In non-bodily ornaments, however, the behaviour creating the structure may serve as an additional source of information to potential partners, providing multiple signals for mate choice. We tested whether and to what extent females use these signals for choosing males by observing the individual sampling behaviour of female Cyathopharynx furcifer in the field. In addition, we experimentally manipulated crater characteristics in the field and laboratory. We found that females spawn preferably with owners of large and well-maintained craters, but when crater size was enlarged or reduced, the resulting building activity of crater owners affected female choice more strongly than the manipulated crater size per se. We discuss the importance of multiple signals in species constructing extended phenotype

Sequential polyandry affords post-mating sexual selection in the mouths of cichlid females

Females mating with multiple males may obtain direct benefits such as nuptial gifts or paternal care or indirect (i.e. genetic) benefits resulting in higher-quality offspring. While direct benefits are easily identified, it is difficult to determine indirect benefits, and it is hence largely unclear how they are obtained. This is particularly true in species with external fertilisation, where females seem to have little control over fertilisation. In cichlids, most maternal mouthbrooders show sequential multiple mating, where females visit several males for egg deposition. Genetic data revealed that multiple paternity of eggs and young in the mouth of females is common, but behavioural data of female spawning decisions are missing. Here, we test four hypotheses to explain female multiple mating in the maternally mouthbrooding cichlid, Ophthalmotilapia ventralis: (1) fertilisation insurance, (2) genetic bet-hedging, (3) female choice and (4) ‘sperm shopping' (i.e. induction of sperm competition resulting in sexually selected sperm). Detailed observations of spawning behaviour in the field combined with histological analyses of the male reproductive organs suggest that fertilisation insurance, genetic bet-hedging and pre-mating female choice are unlikely to explain the sequential female multiple mating in O. ventralis. Instead, cryptic female choice by sperm shopping, i.e. post-mating sexual selection, is most compatible with our data and might be the major ultimate cause of multiple mating in females of this species and of mouthbrooding cichlids with maternal care in general. Our study provides new insight into ultimate causes of sequential polyandry in species with external fertilisation, as hitherto post-mating sexual selection by cryptic female choice has been assumed to be incompatible with external fertilisation mechanisms except by components of the ovarian flui

Sexual conflict over breeding substrate causes female expulsion and offspring loss in a cichlid fish

Females of the Lake Tanganyika cichlid Lamprologus callipterus exclusively breed in empty snail shells that males collect in their territories. Male-male competition for shells is severe, leading to frequent shell stealing and territory takeover. As a consequence, males have breeding females in their shells that spawned with competitors. In this field study, we investigated both naturally occurring and experimentally induced encounters of territorial males with females that had spawned with other males. We found that the breeding success of females that were taken over by a different male was significantly reduced. Behavioral observations after experimental shell relocation further showed that males recognized females that they had not spawned with: males directed more exploration and manipulation behavior toward such shells compared with controls. Reoccupation rate of emptied experimental shells was significantly higher than that of unmanipulated empty shells. This indicates that shell stealing and nest takeover, followed by female expulsion, contribute to the reproductive success of L. callipterus males. We also found that female mate choice reduces expulsion risk: females preferred to mate with large males, and male size correlated with dominance. We conclude that the limited availability of breeding substrate is a key determinant of both intrasexual competition and intersexual conflict in this specie

Alternative reproductive tactics in snail shell-brooding cichlids diverge in energy reserve allocation

Life history theory predicts that the amount of resources allocated to reproduction should maximize an individual's lifetime reproductive success. So far, resource allocation in reproduction has been studied mainly in females. Intraspecific variation of endogenous energy storage and utilization patterns of males has received little attention, although these patterns may vary greatly between individuals pursuing alternative reproductive tactics (ARTs). ARTs are characterized by systematic variation of behavioral, physiological, and often morphological traits among same-sex conspecifics. Some individuals may rely on previously accumulated reserves, because of limited foraging opportunities during reproduction. Others may be able to continue foraging during reproduction, thus relying on reserves to a lesser extent. We therefore predicted that, if male tactics involve such divergent limitations and trade-offs within a species, ARTs should correspondingly differ in energy reserve allocation and utilization. To test this prediction, we studied short-term and long-term reserve storage patterns of males in the shell-brooding cichlid Lamprologus callipterus. In this species, bourgeois males investing in territory defense, courtship, and guarding of broods coexist with two distinct parasitic male tactics: (1) opportunistic sneaker males attempting to fertilize eggs by releasing sperm into the shell opening when a female is spawning; and (2) specialized dwarf males attempting to enter the shell past the spawning female to fertilize eggs from inside the shell. Sneaker males differed from other male types by showing the highest amount of accumulated short-term and long-term fat stores, apparently anticipating their upcoming adoption of the nest male status. In contrast, nest males depleted previously accumulated energy reserves with increasing nest holding period, as they invest heavily into costly reproductive behaviors while not taking up any food. This conforms to a capital breeder strategy. Dwarf males did not accumulate long-term fat stores at all, which they can afford due to their small behavioral effort during reproduction and their continued feeding activity, conforming to an income breeder strategy. Our data confirm that the resource storage patterns of males pursuing ARTs can diverge substantially, which adds to our understanding of the coexistence and maintenance of alternative reproductive patterns within species

Predators, reproductive parasites, and the persistence of poor males on leks

Lekking males are thought to face strong directional selection on secondary sexual traits. How variation in male traits can persist under these conditions remains problematic (the lek paradox). Here, we present several game-theoretic models that show that avoidance of costly and mobile predators, sneakers, or brood parasites (enemies) leads to variation in female choice. This can result in maintenance of variation in male quality. "Enemies” will congregate around higher quality males. Females must then trade-off the benefits of mating with high-quality males against the increased risk of enemies. At equilibrium, the models predict a positive correlation between the quality of a male and the proportions of both enemies and females visiting him. In the first model, we use this framework to predict the lowest quality male on the lek that will receive any matings. In the second model, we examine the influence of this female-enemy game on the maintenance of variation in male quality. Low-quality males are likely to persist when enemies are costly to females or occur at high density, and when there is some spatial structure on the lek, so that neighboring males are typically of similar quality. If enemies are more costly to males than to females, high-quality males may benefit from receiving fewer female visits. In the third model, we consider the special case when enemies are male reproductive parasites. These models illustrate the importance of considering the simultaneous decisions of multiple players in mate choice game

Experimental evidence for helper effects in a cooperatively breeding cichlid

Neolamprologus pulcher is a cooperatively breeding cichlid fish, in which helpers stay in their natal territory and help with brood care, territory defense, and maintenance. In this study we investigated helper effects by an experimental group size reduction in the field. After this manipulation, focal helpers in reduced groups tended to feed less, and small helpers visited the breeding shelter significantly more often than same-sized helpers in control groups. No evidence was found that remaining helpers compensated for the removed helpers by increasing territory defense and maintenance behavior. Breeders, however, did show a lower defense rate, possibly caused by an increase in brood care effort. Survival of fry was significantly lower in removal than control groups, which provides the first experimental proof in a natural population of fish that brood care helpers do effectively help. The data suggest that in small, generally younger, helpers, kin selection may be an important evolutionary cause of cooperation. Large helpers, however, who are generally older and less related to the breeders than small helpers are suggested to pay to be allowed to stay in the territory by helping. All group members benefit from group augmentatio

Costs of delayed dispersal and alloparental care in the fungus-cultivating ambrosia beetle Xyleborus affinis Eichhoff (Scolytinae: Curculionidae)

Body reserves may determine the reproductive output of animals, depending on their resource allocation strategy. In insects, an accumulation of reserves for reproduction is often obtained before dispersal by pre-emergence (or maturation) feeding. This has been assumed to be an important cause of delayed dispersal from the natal nest in scolytine beetles. In the cooperatively breeding ambrosia beetles, this is of special interest because in this group delayed dispersal could serve two alternative purposes: "selfish” maturation feeding or "altruistic” alloparental care. To distinguish between these two possibilities, we have experimentally studied the effect of delayed dispersal on future reproductive output in the xyleborine ambrosia beetle Xyleborus affinis. Females experimentally induced to disperse and delayed dispersing females did not differ in their body condition at dispersal and in their founding success afterwards, which indicates that females disperse independently of condition, and staying adult females are fully mature and would be able to breed. However, induced dispersers produced more offspring than delayed dispersers within a test period of 40days. This suggests that delayed dispersal comes at a cost to females, which may result primarily from alloparental care and leads to a reduced reproductive output. Alternatively, females might have reproduced prior to dispersal. This is unlikely, however, for the majority of dispersing females because of the small numbers of offspring present in the gallery when females dispersed, suggesting that mainly the foundress had reproduced. In addition, "gallery of origin” was a strong predictor of the reproductive success of females, which may reflect variation in the microbial complex transmitted vertically from the natal nest to the daughter colony, or variation of genetic quality. These results have important implications for the understanding of proximate mechanisms selecting for philopatry and alloparental care in highly social ambrosia beetles and other cooperatively breeding arthropod

Fungus Cultivation by Ambrosia Beetles: Behavior and Laboratory Breeding Success in Three Xyleborine Species

Fungus cultivation by ambrosia beetles is one of the four independently evolved cases of agriculture known in animals. Such cultivation is most advanced in the highly social subtribe Xyleborina (Scolytinae), which is characterized by haplodiploidy and extreme levels of inbreeding. Despite their ubiquity in forests worldwide, the behavior of these beetles remains poorly understood. This may be in part because of their cryptic life habits within the wood of trees. Here we present data obtained by varying a laboratory breeding technique based on artificial medium inside glass tubes, which enables behavioral observations. We studied species of the three most widespread genera of Xyleborina in the temperate zone: Xyleborus, Xyleborinus, and Xylosandrus. We raised several generations of each species with good breeding success in two types of media. The proportion of females of Xyleborinus saxesenii Ratzeburg producing offspring within 40 d depended significantly on founder female origin, which shows a transgenerational effect. Labor-intensive microbial sterilization techniques did not increase females' breeding success relative to a group of females shortly treated with ethanol. Gallery productivity measured as the mean number of mature offspring produced after 40 d varied between species and was weakly affected by the type of medium used and foundress origin (field or laboratory) in X. saxesenii, whereas different preparation and sterilization techniques of the beetles had no effect. Behavioral observations showed the time course of different reproductive stages and enabled to obtain detailed behavioral information in all species studied. We propose that the laboratory techniques we describe here are suited for extensive studies of sociality and modes of agriculture in the xyleborine ambrosia beetles, which may yield important insights into the evolution of fungal agriculture and advanced social organizatio