Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, <Emphasis Type="Italic">Megalopta genalis</Emphasis> (Halictidae)

Developmental maternal effects are a potentially important source of phenotypic variation, but they can be difficult to distinguish from other environmental factors. This is an important distinction within the context of social evolution, because if variation in offspring helping behavior is due to maternal manipulation, social selection may act on maternal phenotypes, as well as those of offspring. Factors correlated with social castes have been linked to variation in developmental nutrition, which might provide opportunity for females to manipulate the social behavior of their offspring. Megalopta genalis is a mass-provisioning facultatively eusocial sweat bee for which production of males and females in social and solitary nests is concurrent and asynchronous. Female offspring may become either gynes (reproductive dispersers) or workers (non-reproductive helpers). We predicted that if maternal manipulation plays a role in M. genalis caste determination, investment in daughters should vary more than for sons. The mass and protein content of pollen stores provided to female offspring varied significantly more than those of males, but volume and sugar content did not. Sugar content varied more among female eggs in social nests than in solitary nests. Provisions were larger, with higher nutrient content, for female eggs and in social nests. Adult females and males show different patterns of allometry, and their investment ratio ranged from 1.23 to 1.69. Adult body weight varied more for females than males, possibly reflecting increased variation in maternal investment in female offspring. These differences are consistent with a role for maternal manipulation in the social plasticity observed in M. genalis.     

Philopatry and nest founding in a primitively social bee,Halictus rubicundus

Summary Observations of inter- and intraseasonal dispersal patterns in the primitively social sweat bee Halictus rubicundus in New York reveal considerable philopatry in both sexes. Females overwinter away from the nest aggregation, in diapause for 8–11 months, and return to dig new nests close to the site of their natal nests (typically within 50 cm). Nests are all founded by siggle females (haplometrosis). Clumping of nests may reflect patterns of soil vegetation. Workers rarely enter or take up residence in non-natal nests. Males commonly return to both natal and non-natal nests, and actively patrol vegetation near the natal aggregation for females. These philopatric tendencies, in combination with the haplometrotic mode of nest founding, should have important effects on population structure, particularly in terms of population subdivision, mate choice, and intracolony interactions. The resulting population structure may be conducive to the evolution and maintenance of social behavior.     

Assured fitness returns favor sociality in a mass-provisioning sweat bee,Megalopta genalis (Hymenoptera: Halictidae)

Assured fitness returns models for the evolution of sociality emphasize the selective value of ensuring that offspring receive adequate parental care to reach maturity. If a member of a social group dies, it can accrue returns on investment in offspring through the efforts of surviving social partners. We provide evidence that in the mass-provisioning, facultatively social sweat bee Megalopta genalis, adult presence in the nest throughout brood development provides protection from ant predation. Nests with adults present were well protected, and brood in nests with adults removed suffered higher predation. Females in observation nests showed effective defensive behavior against experimentally introduced ants, and bees in natural nests repulsed naturally occurring ant raids. Megalopta nest architecture and behavior are such that the brood of several cooperating females can be defended with little additional cost relative to solitary nesting. The benefits of cooperative defense may favor group living in mass provisioning bees. Our observations and experiments suggest that parental care throughout brood development can be adaptive in mass provisioning species, supporting the predictions of assured fitness returns models.     

Solitary behavior in a high-altitude population of the social sweat bee Halictus rubicundus (Hymenoptera: Halictidae)

In the subalpine region of the Rocky Mountains of Colorado, United States, Halictus rubicundus has a solitary life cycle, but it is social in other parts of its known range. The brood is protandrous, with a nearly equal investment in the sexes. Productivity averages 6.5 offspring per foundress female, similar to the second brood of social nests in New York, but less than the combined productivity of both New York broods. Leucophora sp. (Diptera: Anthomyiidae) is the principal cause of brood mortality in Colorado. Foundress females in about half the nests survive until brood emerge as adults. Retention of these foundresses decreases offspring mortality by 68%. Comparable abilities to express solitary behavior with a single brood may characterize other eusocial halictine lineages that have successfully invaded high altitudes in the Rocky Mountains. The apparent inability to do this may help explain the absence of other eusocial halictine bees and polistine wasps at high altitudes, despite their success at lower elevations in the same mountains. Presence or absence of this ability may help explain latitudinal distributions of these lineages in North America. Holarctic distributions of lineages with eusocial behavior can be explained by migration as solitary populations from Eurasia to North America across Pleistocene Bering land bridges, with re-expression of double-brooded, eusocial behavior when the species then extended their ranges southward in North America. Received: 4 November 1994/Accepted after revision: 23 October 1995     

Parent-offspring resemblance in degree of sociality in a passerine bird

The tendency to aggregate with conspecifics is a common type of social behavior, and interspecific differences in degree of sociality may indicate that evolutionary changes in sociality have been shaped by past selection pressures. A pre-requisite for such evolutionary change is that the behavior in question has an additive genetic basis. I investigated parent-offspring resemblance in two characteristics of sociality (colony size and nearest neighbor distance) in the semi-colonial barn swallow Hirundo rustica. Heritability estimates of these phenotypic characters were statistically significant. Offspring that were transferred to foster nests as part of brood size manipulation or cross-fostering experiments resembled their original parents more than their foster parents with respect to sociality. There was little evidence of phenotypic characteristics of mothers being significantly related to colony size or nearest neighbor distance of their offspring. Maintenance of genetic variation in sociality in this species may be related to the facts that the relationship between reproductive success and colony size differs among years, and that individuals differing in phenotypic quality have different optimal colony sizes.     

Intra-colony relatedness and sociality in the allodapine bee Exoneura bicolor

Summary Overwintered and newly co-founded nests of Exoneura bicolor exhibit different grades of sociality. Intra-colony relatedness was estimated for adults and female brood in both nest types using allozyme data and a multiallelic estimator. The higher relatedness among female brood from overwintered nests compared to newly-founded nests is consistent with the difference in sociality between these colony types (semisocial versus quasisocial). However, intra-colony relatedness among adults is higher in cofounded nests than in overwintered nests, suggesting that differences in sociality are determined by benefit/cost ratios associated with non-reproductive strategies, rather than relatedness between interactants. Rapid egg-production in newly founded nests allows eggs to be stockpiled. This reduceds the tasks available to non-reproductives in early phases of colony development and limits the payoffs available for reproductive altruism. It is suggested that the social flexibility characteristic of allodapines is a consequence of communal progressive rearing which allows many benefits from cooperative nesting to be gained without worker sterility.     

Foundress polyphenism and the origins of eusociality in a facultatively eusocial sweat bee, Megalopta genalis (Halictidae)

The reproductive (queen) and nonreproductive (worker) castes of eusocial insect colonies are a classic example of insect polyphenism. A complementary polyphenism may also exist entirely among females in the reproductive caste. Although less studied, reproductive females may vary in behavior based on size-associated attributes leading to the production of daughter workers. We studied a bee with flexible social behavior, Megalopta genalis, to better understand the potential of this polyphenism to shape the social organization of bee colonies and, by extension, its role in the evolution of eusociality. Our experimental design reduced variation among nest foundresses in life history variables that could influence reproductive decisions, such as nesting quality and early adulthood experience. Within our study population, approximately one third of M. genalis nests were eusocial and the remaining nests never produced workers. Though they do not differ in survival, nest-founding females who do not attempt to produce workers (which we refer to as the solitary phenotype) are significantly smaller and become reproductive later than females who attempt to recruit workers (the social phenotype). Females with the social phenotype are more likely to produce additional broods but at a cost of having some of their first offspring become nonreproductive workers. The likelihood of eusocial organization varies with body size across females of the social phenotype. Thus, fitness consequences associated with size-based plasticity in foundress behavior has colony level effects on eusociality. The potential for size-based polyphenisms among reproductive females may be an important factor to consider in the evolutionary origins of eusociality.     

Supplemental food affects egg size but not hatching asynchrony in rollers

Maternal effects can function as a mechanism of transgenerational plasticity by which the environment experienced by parents is translated into the offspring phenotype and fitness. In birds, parents may affect the competitive ability of their offspring, and hence their fitness, by modifying their hatching pattern and/or egg size. However, little is known about how mothers can modify offspring phenotypes and their fitness in response to a sudden change in environmental conditions during egg-laying. Here, we studied the effect of supplemental food during egg-laying on hatching asynchrony and egg size in the Eurasian roller (Coracias garrulus), a species with marked hatching asynchrony. We also explored the effects of maternal investment on offspring fitness. Food supplementation did not affect hatching asynchrony. However, females in food-supplemented nests laid eggs that increased in size with laying order except for an ultimate small egg. Meanwhile, size of eggs laid by females in control nests did not change with laying order. Supplemental food positively affected hatchability of the egg laid just before the last one and negatively affected hatchability of the last laid egg, which seemed to be a side effect of egg size. Consequently, food-supplemented nests produced fewer fledglings and had higher probabilities of suffering brood reduction than control nests. We conclude that egg size in rollers is a plastic trait, sensitive to short-term changes in food conditions. Furthermore, our results show that maternal investment in egg size may potentially affect offspring fitness.     

The habitat saturation hypothesis and sociality in an allodapine bee: cooperative nesting is not “making the best of a bad situation”

Several factors thought to be important for the evolution of cooperative breeding in vertebrates have received little attention in facultatively social insects. One of these, the “habitat saturation hypothesis” of Selander (1964), predicts that colony sizes will be greater in breeding units where dispersal opportunities are limited, suggesting that group living is a secondary option to independent reproduction. The Australian allodapine bee Exoneura bicolor exhibits a number of traits that occur in cooperatively breeding bird species, including long life-span, repeated opportunities for reproduction, and vulnerability to brood predation and parasitism. We experimentally examined the effect of a potentially limiting environmental factor, nesting substrate availability, as an agent influencing sociality in E. bicolor. We manipulated nesting substrate availability in two separate locations during a time when foundress dispersal is common. No significant difference was found between colony sizes in cases where dispersal options were abundant and cases where dispersal options were limited. An increase in opportunities for dispersal did not lead to higher rates of independent nesting, suggesting that cooperative nesting is a preferred strategy regardless of distance-related costs of dispersal. Reproductivity per female and brood survival were examined as factors selecting for group living. Low survival of brood in single-female nests has the potential to select for cooperative nesting in this bee. Received: 29 September 1995/Accepted after revision: 24 June 1996     

Context-dependent genetic benefits of extra-pair mate choice in a socially monogamous passerine

Extra-pair paternity is common in socially monogamous passerines; however, despite considerable research attention, consistent differences in fitness between within-pair offspring (WPO) and extra-pair offspring (EPO) have not been demonstrated. Recent evidence indicates that differences between maternal half-siblings may depend on environmental conditions, but it is unclear whether the influence of paternal genetic contribution should be most apparent under comparatively poor or favourable conditions. We compared phenotypic characteristics of WPO and EPO in 30 mixed-paternity broods of the tree swallow (Tachycineta bicolor) in relation to experimentally increased nest temperature (n = 13 heated nests; 17 control nests) and natural abundance of haematophagous parasites (Protocalliphora spp.). This allowed us to test the hypothesis that genetic benefits of extra-pair mating are environment dependent. EPO grew their ninth primary feathers faster than WPO regardless of nest temperature or parasite load and had significantly longer ninth primary feathers at fledging when parasite abundance was low, and when they were positioned early in the hatching sequence relative to WPO. In contrast, WPO under similar conditions did not differ from EPO in any phenotypic trait measured. These results indicate that the fitness benefits of extra-pair mating are likely to be context dependent, and that genetic effects on some phenotypic traits may be more apparent when conditions are relatively favourable.     

The sociality of Xylocopa pubescens: does a helper really help?

Summary Solitary and social nests of the facultatively social carpenter bee Xyclopa pubescens can be found simultaneously during the major part of the breeding season. Social nests contain a reproductively dominant forager and either her adult offspring or a formerly reproductive, guarding female. The costs and benefits to the dominant animal of allowing a defeated female to remain as a guard in the nest were analysed in terms of brood loss and brood gain. The costs included the probability that the guard would regain reproductively dominant status. The most important benefits were the protection that a guard provided against pollen robbery by conspecifics and the longer foraging time available to a forager when her nest was protected. The balance between costs and benefits depended on the severity of ecological constraints. During certain periods of intense competition for pollen or nests, the benefits clearly outweighed the costs.Correspondence to: K. Hogendoorn     

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 organization.     

Indiscriminate care of offspring predates the evolution of sociality in alloparenting social spiders

Alloparental care—the care of other’s offspring—is a key aspect of sociality in many groups of animals. Understanding how this complex behavior arises requires identifying both the selective forces that may favor it, as well as characteristics of particular lineages that facilitate or hinder its evolution. One potential hindrance is the existence of discrimination against foreign offspring, an obstacle that would need to be overcome in order for alloparental care to evolve. In this study, we explored whether offspring discrimination may have constrained the evolution of alloparental care in social spiders in the genus Anelosimus. Social spiders are known for their cooperative behaviors, which include alloparental care. After quantitatively assessing the extent of alloparenting in the care of egg sacs in natural nests of these spiders, we investigated whether discrimination against foreign egg sacs existed in ancestral pre-social species in the genus. We did so by testing for discrimination between a female’s own and foreign egg sacs in three subsocial sister taxa of each social species investigated. We found no detectable evidence of discrimination in the care of egg sacs by female Anelosimus, regardless of level of sociality. We used these data, along with those from previous studies, to infer that a lack of discrimination is likely the ancestral state in the genus Anelosimus. This supports the idea that offspring discrimination was not a constraint on the evolution of alloparental care in social Anelosimus species. We discuss the evolutionary implications of this finding, and suggest that lack of offspring discrimination may have eased the transition from solitary to cooperative breeding.     

Do female black-capped chickadees prefer high-ranking males as extra-pair partners?

Previous studies have shown that some female black-capped chickadees (Poecile atricapillus) solicit copulations from males that rank higher in winter flocks than their social mates, and extra-pair paternity in nests occurs commonly enough to be considered a potential female mating tactic. This study uses blood samples collected in 1992–1995 from 58 families of black-capped chickadees to test whether females with extra-pair offspring have chosen extra-pair sires higher in social rank than their mates. Paternity was assessed with multilocus DNA fingerprinting in 1992–1994 nests and with microsatellite and single-locus minisatellite DNA typing in 1995 nests. Seventeen of 58 nests (29.3%) contained young genetically mismatched with their social father. In 11 of 15 cases where the identity of the extra-pair male was known, the extra-pair male was dominant to the social father. Using data from 29 nests located in 1994 and 1995 for which we had the most data on relative ranks of males, high-ranking males had greater realized reproductive success than low-ranking males as a result of extra-pair fertilizations. There was no significant difference between the number of nests containing extra-pair young of females mated to low-ranked versus high-ranked males. Two nests in 1995 contained young either genetically mismatched with both social parents (intraspecific brood parasitism) or, in one nest, genetically mismatched with the social mother but not the social father (quasi-parasitism). The implications of female strategies acquiring genetic benefits through extra-pair copulations are discussed. Received: 7 July 1997 / Accepted after revision: 14 March 1998     

Parental facilitation: parent-offspring relations in communally breeding birds

Summary A view of parent-offspring relations is developed that stresses an increased role for mutualism and tolerance rather than conflict in evolutionary trends toward sociality. For example, in Aphelocoma jays, parental tolerance of offspring increases from asocial to social species, contrary to what parental manipulation or parent-offspring conflict models have suggested. A simple model is presented in which parents can leave more grand-offspring while having fewer offspring through a mutualistic relationship between parent and offspring. Consistent with the model are the following observations: (1) At the extreme of sociality, in Mexican jays, A. ultramarina, both sexes commonly inherit their natal territory, thus retaining productive territories largely under control of genotypes that tolerate persistence of young in the territory. Sons and daughters may breed on their natal territory in the presence of their mothers and presumed fathers. (2) Jays banded as nestlings in the study area achieved higher reproductive success when breeding on their natal territory than those that moved to other territories. It is hypothesized that plural breeding can evolve as an extension of the trend leading to singular breeding via a non-altruistic reduction in the number of offspring per parent. The concept of parental facilitation may prove to be important for many highly social types of animals, including insects, birds and mammals.     

Evolution of Nesting Height in an Endangered Hawaiian Forest Bird in Response to a Non‐Native Predator

Abstract: The majority of bird extinctions since 1800 have occurred on islands, and non‐native predators have been the greatest threat to the persistence of island birds. Island endemic species often lack life‐history traits and behaviors that reduce the probability of predation and they can become evolutionarily trapped if they are unable to adapt, but few studies have examined the ability of island species to respond to novel predators. The greatest threat to the persistence of the Oahu Elepaio (Chasiempis ibidis), an endangered Hawaiian forest bird, is nest predation by non‐native black rats (Rattus rattus). I examined whether Oahu Elepaio nest placement has changed at the individual and population levels in response to rat predation by measuring nest height and determining whether each nest produced offspring from 1996 to 2011. Average height of Oahu Elepaio nests increased 50% over this 16‐year period, from 7.9 m (SE 1.7) to 12.0 m (SE 1.1). There was no net change in height of sequential nests made by individual birds, which means individual elepaios have not learned to place nests higher. Nests ≤3 m off the ground produced offspring less often, and the proportion of such nests declined over time, which suggests that nest‐building behavior has evolved through natural selection by predation. Nest success increased over time, which may increase the probability of long‐term persistence of the species. Rat control may facilitate the evolution of nesting height by slowing the rate of population decline and providing time for this adaptive response to spread through the population.     

Correlates of female choice in resource-defending antelope

Summary Where males offer their mates assistance in rearing offspring as well as access to defended resources, female mate choice should be influenced by both male phenotype and resource quality. In contrast, where there is no paternal care the relative importance of choice for male and territory traits is less well understood. We looked at female distribution across male territories in order to assess mate choice criteria in puku Kobus vardoni, and topi Damaliscus lunatus, two antelope where males defend resources but are not involved in parental care. In both species female distribution was correlated with male phenotype as well as the quality of forage and risk of predation on different territories. Male and territory characteristics were intercorrelated, but statistical analysis revealed that male traits, forage quality and predation risk were all significant, independent predictors of female choice in both study species. This is the first demonstration that female choice in mammals might be simultaneously influenced by male phenotype as well as the quality of defended resources.Correspondence to: A. Balmford     

Diel and lunar patterns of reproduction in the Caribbean and Pacific sergeant major damselfishes Abudefduf saxatilis and A. troschelii

Diel and lunar reproductive patterns of the Caribbean and Pacific sergeant major damselfishes Abudefduf saxatilis and A. troschelii respectively, were studied i the San Blas and Northern Perls Islands of Panama in 1981 and 1982. These are sister-species that have diverged since the uplift of the isthmus of Panama. Caribbean A. saxatilis females typically complete spawning in the nests of males earlier in the morning than do Pacific A. troschelii females. Spawning is rarely observed during the afternoon. Hatching occurs four or five days after spawning in the Caribbean species, and after four days in the Pacific species. In both, fry hatch during the hour following sunset. There also are differences in lunar patterns of spawning between the two species. The Caribbean A. saxatilis spawns throughout the month, exhibiting no lunar periodicity. In the Pacific A. troschelii spawns within nine days on either side of new moon. During the wet season, reproductive activity at a site spans three or four days, but is extended to eight or more days during dry season upwelling in the Bay of Panama. Thus, reproductive synchrony is much greater within than between colonies of the Pacific sergeant major, particularly in the wet season. Reproductive synchrony in the Pacific sergeant major might be beneficial because fry hatching at dusk encounter favorable tides for transport away from reef-based predators around new moon, or because reproductive synchrony reduces the risk of predation on unhatched embryos in nests guarded by males. Tidal amplitude and the rate of predation on embryos in nests are greater in the Pacific.     

Negative correlation between male ornament size and female preference intensity in a wild guppy population

Although traditional sexual selection theories for the evolution of ornamental male traits often assume consistency in female preferences for the traits over time, recent theories predict plasticity in female mate preferences and the contribution of plastic female preferences to the maintenance of polymorphism in male sexual ornaments. However, the plasticity of female preferences and its influences on male ornaments are almost unknown in natural populations. Here we examined both the intensity of female preferences and the exaggeration of a male ornament (relative area of orange spots) in a wild population of the guppy (Poecilia reticulata) every few months over a period of 3 years. Results indicated that female preference intensity was negatively correlated with the relative area of orange spots of males. In addition, we found a positive correlation between female preference intensity and the relative area of orange spots of males of their offspring generation. Because the relative area of orange spots of male guppies is a heritable trait, female preferences might have a strong influence on male orange spot size in the next generation. This study provides the first evidence of plastic female preferences depending on the scarcity of males with large ornaments in a natural population. Results of this study imply a possible contribution of female preferences for the maintenance of variation in male ornamentation.     

Sociogenetic organization of the red ant Myrmica rubra

Knowledge of the sociogenetic organization determining the kin structure of social insect colonies is the basis for understanding the evolution of insect sociality. Kin structure is determined by the number and relatedness of queens and males reproducing in the colonies, and partitioning of reproduction among them. This study shows extreme flexibility in these traits in the facultatively polygynous red ant Myrmica rubra. Relatedness among worker nestmates varied from 0 to 0.82. The most important reason for this variation was the extensive variation in the queen number among populations. Most populations were moderately or highly polygynous resulting in low relatedness among worker nestmates, but effectively monogynous populations were also found. Polygynous populations also often tend to be polydomous, which is another reason for low relatedness. Coexisting queens were positively related in two populations out of five and relatedness was usually similar among workers in the same colonies. Due to the polydomous colony organization and short life span of queens, it was not possible to conclusively determine the importance of unequal reproduction among coexisting queens, but it did not seem to be important in determining the relatedness among worker nestmates. The estimates of the mating frequency by queens remained ambiguous, which may be due to variation among populations. In some populations relatedness among worker nestmates was high, suggesting monogyny and single mating by queens, but in single-queen laboratory nests relatedness among the worker offspring was lower, suggesting that multiple mating was common. The data on males were sparse, but indicated sperm precedence and no relatedness among males breeding in the same colony. A comparison of social organizations and habitat requirements of M. rubra and closely related M. ruginodis suggested that habitat longevity and patchiness may be important ecological factors promoting polygyny in Myrmica. Received: 15 May 1995/Accepted after revision: 17 October 1995