Genetic influence on caste determination underlying the asexual queen succession system in a termite

The question of how reproductives and sterile workers differentiate within eusocial groups has long been a core issue in the study of social insects. Recent studies have shown that not only environmental factors but also genetic factors affect caste differentiation. In the termite Reticulitermes speratus, queens produce their replacements (neotenics) asexually but use normal sexual reproduction to produce other colony members. Here, we demonstrate a genetic influence on caste determination underlying the asexual queen succession system in this termite species. Thelytoky in termites is accomplished by automixis with terminal fusion, yielding almost completely homozygous offspring; thus, parthenogenetically and sexually produced offspring profoundly differ in heterozygosity. An analysis of the relationship between the reproductive dominance of female neotenics obtained from experimentally orphaned colonies and their genotypes at five microsatellite loci showed that homozygosity at two loci influenced the developmental priority and/or reproductive quality of neotenics. These results suggest the existence of a multi-locus system affecting the queen fecundity and explain why parthenogens have genetic priority to become neotenics in this termite species.     

Queen number, queen cycling and queen loss: the evolution of complex multiple queen societies in the social wasp genus Ropalidia

Complex, highly integrated societies have evolved from simpler societies repeatedly, and the social insects provide an excellent model system for understanding increasing complexity and integration. In the paper wasps, large societies, known as swarm-founding, have evolved repeatedly from smaller societies, known as independent-founding. Swarm-founding colonies have many more queens than independent-founding colonies, which should dramatically reduce relatedness, posing a challenge to cooperation. However, in each instance, swarm-founding species have also evolved a cyclical pattern of queen reduction which elevates relatedness despite high queen numbers. The genus Ropalidia provides an excellent system in which to study the transition to swarm-founding because it has both independent and swarm-founding species. We studied the Australian independent-founding wasp Ropalidia revolutionalis to better understand the evolution of multiple queens and their periodic reductions in swarm-founding wasps. Using microsatellite genetic markers we genotyped queens, workers and brood from 37 colonies and found that while most colonies had a single queen, three of the colonies had multiple queens at or immediately prior to the time of collection. An additional seven colonies had had multiple co-occurring queens earlier in the season. We also found that colonies experienced many queen losses, and that founding queens were gradually lost until they were replaced by a new cohort of daughter queens in many colonies. This pattern is similar to the periodic reductions and replacements in swarm-founding wasps and suggests that multiple queens and queen cycling evolved relatively early in the shift to swarm-founding in Ropalidia.Communicated by R. Page     

Lack of evidence for nepotism by workers tending queens of the polygynous termite <Emphasis Type=Italic>Nasutitermes corniger</Emphasis>

Kin selection theory predicts that workers in social insect colonies should preferentially aid close relatives over less related or unrelated individuals if such behaviors increase inclusive fitness. For example, a worker in a polygynous (multiple-queen) colony is predicted to tend its own mother rather than an unrelated queen if this nepotistic behavior increases its mother’s reproductive success in excess of costs. Despite predictions, experimental tests conducted in the social Hymenoptera have found no clear evidence of nepotism. No tests for nepotism have been carried out in the Isoptera (termites), another major insect taxon showing highly developed sociality. We tested for nepotistic behavior in the termite Nasutitermes corniger by determining if workers preferentially fed and groomed their mothers in a laboratory assay. We collected workers from nine naturally occurring multiple-queen colonies as they tended queens and determined their parentage using highly variable microsatellite markers. Our results provide no evidence that workers tend their mothers in preference to co-occurring queens. The absence of evidence for nepotism is consistent with previous results reported from numerous studies of eusocial hymenopterans.     

Transgenerational plasticity in the sea: context-dependent maternal effects across the life history

Maternal effects can have dramatic influences on the phenotype of offspring. Maternal effects can act as a conduit by which the maternal environment negatively affects offspring fitness, but they can also buffer offspring from environmental change by altering the phenotype of offspring according to local environmental conditions and as such, are a form of transgenerational plasticity. The benefits of maternal effects can be highly context dependent, increasing performance in one life-history stage but reducing it in another. While maternal effects are increasingly well understood in terrestrial systems, studies in the marine environment are typically restricted to a single, early life-history stage. Here, I examine the role of maternal effects across the life history of the bryozoan Bugula neritina. I exposed maternal colonies to a common pollution stress (copper) in the laboratory and then placed them in the field for one week to brood offspring. I then examined the resistance of offspring to copper from toxicant-exposed and toxicant-na?ve mothers and found that offspring from toxicant-exposed mothers were larger, more dispersive, and more resistant to copper stress than offspring from na?ve mothers. However, maternal exposure history had pervasive, negative effects on the post-metamorphic performance (particularly survival) of offspring: offspring from toxicant-exposed mothers had poorer performance after six weeks in the field, especially when facing high levels of intraspecific competition. Maternal experience can have complex effects on offspring phenotype, enhancing performance in one life-history stage while decreasing performance in another. The context-dependent costs and benefits associated with maternally derived pollution resistance may account for why such resistance is induced rather than continually expressed: mothers must balance the benefits of producing pollution-resistant larvae with the costs of producing poorer performing adults (in the absence of pollution).     

Relatedness,recognition errors,and colony fusion in the termite <Emphasis Type="Italic">Nasutitermes corniger</Emphasis>

Loss of aggression between social groups can have far-reaching effects on the structure of societies and populations. We tested whether variation in the genetic structure of colonies of the termite Nasutitermes corniger affects the probability of aggression toward non-nestmates and the ability of unrelated colonies to fuse. We determined the genotypes of workers and soldiers from 120 colonies at seven polymorphic microsatellite loci. Twenty-seven colonies contained offspring of multiple founding queens or kings, yielding an average within-colony relatedness of 0.33. Genotypes in the remaining 93 colonies were consistent with reproduction by a single queen and king or their progeny, with an average within-colony relatedness of 0.51. In standardized assays, the probability of aggression between workers and soldiers from different colonies was an increasing function of within-colony relatedness. The probability of aggression was not affected significantly by the degree of relatedness between colonies, which was near zero in all cases, or by whether the colonies were neighbors. To test whether these assays of aggression predict the potential for colony fusion in the field, we transplanted selected nests to new locations. Workers and soldiers from colonies that were mutually tolerant in laboratory assays joined their nests without fighting, but workers and soldiers that were mutually aggressive in the assays initiated massive battles. These results suggest that the presence of multiple unrelated queens or kings promotes recognition errors, which can lead to the formation of more complex colony structures.     

Polygyny in the red-winged blackbird: do females prefer monogamy or polygamy?

Five hypotheses have been proposed to explain polygyny in the red-winged blackbird (Agelaius phoeniceus). We categorized the hypotheses into three groups based on female preference for unmated versus monogamously mated males: (1) the “polygyny threshold” model, “sexy son” hypothesis and the “asynchronous settlement” model, which assume that females prefer unmated males to mated males on breeding situations of homogeneous quality; (2) the “neutral mate choice” hypothesis, which assumes that females have no preference; and (3) the “cooperative female choice” model, which assumes that females prefer monogamously mated males to unmated males. We tested the direction of female preference in two field experiments. In both experiments, newly settling females were given a choice of two adjacent territories, one defended by an unmated male and the other by a monogamously mated male. Male mating status was randomized with respect to the variation in territory quality and male quality. Early in the breeding season, significantly more females settled with the unmated males than with the mated males. Although more females settled with the unmated males than with the mated males late in the breeding season, the difference was no longer significant. Female settlement late in the season appeared to be related to the tenure of the resident females: the new females avoided territories where the resident females were in early stages of their nesting, but settled on territories where the resident females were in late stages. The pattern of female settlement shows that females prefer unmated males to mated males. The preference is consistent with the polygyny threshold model, sexy son hypothesis and the asynchronous settlement model, and inconsistent with the neutral mate choice hypothesis and the cooperative female choice model. For this reason, the latter two hypotheses are unlikely to explain the occurrence of polygyny in our population of red-winged blackbirds. Received: 1 December 1994 / Accepted after revision: 28 October 1995     

Incest avoidance,fluctuating asymmetry,and the consequences of inbreeding in Iridomyrmex humilis,an ant with multiple queen colonies

Summary Inbreeding may have important consequences for the genetic structure of social insects and thus for sex ratios and the evolution of sociality and multiple queen (polygynous) colonies. The influence of kinship on mating preferences was investigated in a polygynous ant species, Iridomyrmex humilis, which has within-nest mating. When females were presented simultaneously with a brother that had been reared in the same colony until the pupal stage and an unrelated male produced in another colony, females mated preferentially with the unrelated male. The role of environmental colony-derived cues was tested in a second experiment where females were presented with two unrelated males, one of which had been reared in the same colony until the pupal stage (i.e., as in the previous experiment), while the other had been produced in another colony. In this experiment there was no preferential mating with familiar or unfamiliar males, suggesting that colony-derived cues might not be important in mating preferences. Inbreeding was shown to have no strong effect on the reproductive output of queens as measured by the number of worker and sexual pupae produced. The level of fluctuating asymmetry of workers produced by inbreeding queens was not significantly higher than that of non-inbreeding queens. Finally, colonies headed by inbreeding queens did not produce adult diploid males. Based on the current hypotheses of sex-determination the most plausible explanations for the absence of diploid-male-producing colonies are that (i) workers recognized and eliminated these males early in their development, and/or (ii) there are multiple sex-determining loci in this species. It is suggested that even if inbreeding effects on colony productivity are absent or low, incest avoidance mechanisms may have evolved and been maintained if inbreeding queens produce a higher proportion of unviable offspring. Correspondence to: L. Keller at the present address     

From metamorphosis to maturity in complex life cycles: equal performance of different juvenile life history pathways

Performance in one stage of a complex life cycle may affect performance in the subsequent stage. Animals that start a new stage at a smaller size than conspecifics may either always remain smaller or they may be able to "catch up" through plasticity, usually elevated growth rates. We study how size at and date of metamorphosis affected subsequent performance in the terrestrial juvenile stage and lifetime fitness of spadefoot toads (Pelobates fuscus). We analyzed capture-recapture data of > 3000 individuals sampled during nine years with mark-recapture models to estimate first-year juvenile survival probabilities and age-specific first-time breeding probabilities of toads, followed by model selection to assess whether these probabilities were correlated with size at and date of metamorphosis. Males attained maturity after two years, whereas females reached maturity 2-4 years after metamorphosis. Age at maturity was weakly correlated with metamorphic traits. In both sexes, first-year juvenile survival depended positively on date of metamorphosis and, in males, also negatively on size at metamorphosis. In males, toads that metamorphosed early at a small size had the highest probability to reach maturity. However, because very few toadlets metamorphosed early, the vast majority of male metamorphs had a very similar probability to reach maturity. A matrix projection model constructed for females showed that different juvenile life history pathways resulted in similar lifetime fitness. We found that the effects of date of and size at metamorphosis on different juvenile traits cancelled each other out such that toads that were small or large at metamorphosis had equal performance. Because the costs and benefits of juvenile life history pathways may also depend on population fluctuations, ample phenotypic variation in life history traits may be maintained.     

Studies on the life history of Rhodophysema elegans in laboratory culture

The life history of the red alga Rhodophysema elegans (J. Ag.) Dixon (Peyssoneliaceae: Cryptonemiales), which was commonly found at 4 localities on the south coast of England, has been investigated in laboratory culture. Tetraspores (the only reproductive organs observed) which were derived from field material germinated to repeat the parental tetrasporangiate phase. Sexual reproductive organs were not observed. It is suggested that the probable cause of this direct type of life history is the occurrence of apomeiosis in the sporangial primordium.     

Polygyny in the great reed warbler,Acrocephalus arundinaceus: a possible case of deception

Summary Polygyny was studied for 1 year in a great reed warbler population breeding in southern Germany. Data on various parameters of male and territory characteristics were collected and subjected to multivariate statistical analysis in order to assess their relative importance in female choice. Differences in territory characteristics appeared to be more important (Tab. 1), but there was a strong correlation between male and territory characteristics (Fig. 2, 3). Although the evolutionary advantages of polygyny to males are obvious (Fig. 5), those to females are far from clear. Models based upon the polygyny threshold and sexy son hypotheses predict that females should gain evolutionary advantage in either the short or long-term. Our data did not confirm such predictions, and secondary females showed greatly reduced breeding success (Fig. 4). If females were able to assess the status of mated males, they should instead select unmated males. Great reed warblers are a migrant species with a short breeding cycle in which the male plays relatively little part. They defend large territories in reed beds where visibility is reduced. These factors may permit males to practice a form of deception, by moving and attracting a second female who has little chance to assess that he is already mated.     

The life history of Rhodophysema georgii in laboratory culture

Rhodophysema georgii Batt., a rare epiphyte on Zostera spp., was collected from lowtide-level lagoons at Bembridge (Isle of Wight), and its life history examined in laboratory culture. The tetraspores, the only method of reproduction known, gave rise to small crusts which again developed tetrasporangial sori on the surface, similar to those of the parental material. It is suggested that this direct type of life history is probably due to the repression of meiosis in the tetrasporangial mother cell.     

Replacement of reproductives in Nasutitermes princeps (Desneux) (Isoptera: Termitidae)

Summary The production of replacement reproductives in experimentally orphaned societies was investigated in Nasutitermes princeps (Desneux). From 1 to 180 replacement queens and multiple kings, all adultoids, were found in the 13 nests that were re-collected. Normal imagos, microimagos, or a mixture of the two forms were present, depending on colony composition at the time of orphaning. In colonies with alates, the corresponding forms were found as replacement reproductives. Where only young nymphs were present, microimagos differentiated. Neither the number of queens nor their level of physogastry was correlated with the time elapsed since orphaning, but the total egg-laying rates were. We suggest that competition among queens rather than time determines individual physogastric development. Observations show that the most likely cause of accidental queen death in nature is probably nest fall from the supporting tree. Even in this case, the queen may be able to migrate to a newly rebuilt nest. An experimental simulation of this situation showed that colony migration can occur. The data indicate that the replacement of the primary queen after her accidental death cannot by itself account for the high rate of polygyny (60%) encountered in N. princeps. Two other possible causes are the replacement of the ageing foundress as a normal event of colony life, and colony reproduction by budding off new nests with adultoid reproductives.King Léopold III Biological Station, Laing Island, Papua New Guinea, contribution no. 84Research Assistant of the National Fund for Scientific Research (Belgium)     

Life history consequences of variation in age at primiparity in northern elephant seals

Summary The age when female northern elephant seals, Mirounga angustirostris, bear their first young varies from 2 to 6 years. At Año Nuevo, California, a group of 77 females, primiparous at age 3, had a lower survivorship rate to each successive year up to age 8 than a group of 98 females that deferred initial pupping until age 4. The difference in survivorship appears to be due to the greater relative energetic costs of gestation and lactation incurred by the earlier breeding females during a period in their development when growth is rapid. An alternate hypothesis for the difference in survivorship — that young primiparous females are in poor condition from birth-is untenable; females that pupped early in life were larger at weaning age (a correlate of condition) than females that were primiparous 1 year later.Models based on the data show that differential survival of seals that vary in age at primiparity has important consequences for population growth and life history strategies. The effect of age at primiparity on the rate of increase of populations varies with colony density and juvenile survivorship. The optimal life history strategy for female elephant seals under most conditions existing today, including those at Ano Nuevo during the study period, is to bear the first offspring at age 4. Primiparity at age 3 is projected to be favored when harem density is very low and weaning success and juvenile survivorship are high; postponement of first breeding to age 5 is expected at high harem densities with intense competition for breeding space. Offprint requests to: B.J. Le Boeuf     

On the importance of life history and age structure in biological invasions

The age specific patterns of reproduction and mortality dictated by the life history of an organism apply to potential invaders as well as resident species of an area, but whether certain life history traits are more invasive than others is an unresolved issue. We analyze a two-population system of an invading and a resident species and test the effects of age on the probability to invade when the organisms are iteroparous or semelparous. The life history characteristics of the populations are projected in Leslie matrices, and the probability that the invader exceeds different population sizes is calculated by Monte Carlo analysis. The simulations show that (a) the invasion probability of an iteroparous organism increases with age until the individuals introduced are mature for first reproduction, and then becomes independent of age; (b) the invasion probability is more age sensitive for iteroparous organisms with high juvenile mortality (Type III organisms) than for those with a lower (Type I); (c) invading semelparous organisms are most affected by competition from resident organisms; (d) variations in vital rates of semelparous residents have greater influence on the invasion probability of an iteroparous organism than variations in traits of the invader.     

Polygyny and male parental care in Savannah sparrows: effects on female fitness

Summary To determine the effects of male mating status on female fitness, we compared the reproductive success, survival, and future fecundity of female Savannah sparrows (Passerculus sandwichensis) mated to monogamous vs. polygynous males in a 5-year study on Kent Island, New Brunswick, Canada. The proportion of males with more than one mate varied from 15 to 43% between years and sites. Polygynous and monogamous males fledged young of equal size in every year of the study. Females who shared paternal care with other females laid as many eggs per clutch and clutches per season as monogamously mated females. In most years polygynously mated females showed no delay in laying a second clutch, and they suffered no reduction in fecundity the following year. Recruitment of a female's offspring into the breeding population was generally independent of her mating status. Fitness costs of being mated to a polygynous male were only apparent in one year of the study, during which females mated to polygynous males had higher over-winter mortality than those mated to monogamous males. That same year, young raised by polygynous males were only one-third as likely to survive to reproductive maturity (as inferred by returns) as those raised by monogamous males. A male's mating status had no effect on his own survivorship. A male's mating status did not necessarily reflect his contributions to raising nestlings, which may partially explain why monogamously and polygynously mated females had equal fitness. At 35 nests the proportion of food deliveries brought by individual males varied from 0 to 75%; on average, males brought fewer than 30% of all food deliveries. Yet parental care by polygynous males was no less than that of monogamous males, at least at the nests of their primary females. Secondary females tended to receive less male assistance during the nestling stage, but their reproductive success was indistinguishable from that of primary females. Females feeding young without male assistance made as many food deliveries/h as did pairs in which males brought at least 30% of all food deliveries. Unassisted females did not suffer diminished fledging success or produce smaller fledglings. The benefits of polygyny for male Savannah sparrows are clear: polygynous males recruit more surviving offspring into the breeding population than monogamous males. The fitness of females, on the other hand, appears to be unaffected by whether their mate was monogamous or polygynous except in occasional years. Polygyny may be maintained in this population by the constraints of a female-biased sex ratio, the inability of females to predict a male's paternal care based on his morphology or behavior, the poor correlation between a male's mating status and his assistance at the nest, and inconsistent natural selection against mating with a polygynous male. Correspondence to: N.T. Wheelwright     

Early life history of tropical Anguilla leptocephali in the western Pacific Ocean

In order to examine the early life-history characteristics of tropical eels, otolith microstructure and microchemistry were examined in leptocephali of Anguilla bicolor pacifica (27.6-54.1 mm TL, n=20) and A. marmorata (22.0-47.3 mm TL, n=8) collected during a cruise in the western Pacific. A. bicolor pacifica occurred between 10°N and 15°N in the west and between 5°S and 10°N farther to the east. A. marmorata also occurred in two different latitudinal ranges in the Northern (15-16°N) and Southern Hemispheres (3-15°S) of the western Pacific. The increment widths in the otoliths of these leptocephali increased between the hatch check (0 days) and about an age of 30 days in both species, and then gradually decreased toward the otolith edge. Otolith Sr:Ca ratios showed a gradual increase from the otolith center to the edge. The ages of A. bicolor pacifica and A. marmorata leptocephali ranged from 40 to 128 days and from 38 to 99 days, respectively. Growth rates of A. bicolor pacifica and A. marmorata leptocephali ranged from 0.33 to 0.71 mm day^-1 and from 0.45 to 0.63 mm day^-1, respectively. These leptocephali had estimated growth rates that were spread out throughout most of the reported range of growth rates of the leptocephali of the temperate species, the Japanese eel and the Atlantic eels. Differences in the spatial distribution in relation to current systems, and the age and size compositions of the leptocephali of A. bicolor pacifica and A. marmorata suggested different spawning locations for these two species.     

Observations on the life history of the blue-ringed octopus Hapalochlaena maculosa

The life-history of the blue-ringed octopus Hapalochlaena maculosa (Hoyle) was observed in laboratory aquaria. Eggs from a brooding female were bred through to the next generation. The life cycle lasts approximately 7 months–4 months from hatching to maturity, 1 month from copulation to egg-laying, and an estimated 2 months for embryonic development. This venomous octopus has several unique and interesting habits. Eggs are not attached to a substratum but are carried by the mother throughout their embryonic life. She assumes a brooding posture for the greater part of the time and cradles the eggs between her raised skirt and body. However, she can move froely with her clutch of eggs, conveying them individually or in clusters along her arms from one sucker to the next as occasion demands. Embryos reverse position within their capsules 1 week prior to hatching, and hatch at the distal end of the capsule, mantle-first. Development is direct; there is no planktonic stage. The young immediately assume a benthic habit and, within a few hours, consume the remnant of the yolk-sac which they carry with them from the egg. Juveniles begin to feed on pieces of crab within a week of hatching, and to kill and eat live crabs within a month. They pierce the carapace of their prey at the abdominal articulation and with the aid, apparently, of venom from their posterior salivary glands suck out the partially pre-digested tissues. The ink gland is relatively small in size and is mainly used between the second and the fourth week of juvenile life. Chromatophores begin to function during embryonic life. After hatching there is a progressive change in coloration, and the iridescent blue rings which characterize the species appear at the age of about 6 weeks. Mating is a more active process than has been recorded for other octopuses. The male mounts the female and clasps her securely. After a short struggle the female becomes quite passive, almost inert. Copulation lasts about one hour. The unusual life-history of H. maculosa suggests that it is a highly evolved octopus species. Its direct development, simple diet, and rapid rate of growth make the animal relatively easy to cultivate for experimental or pharmacological purposes.     

Prediction of extinction in plants: interaction of extrinsic threats and life history traits

The global extinction of species proceeds through the erosion of local populations. Using a 60-year time series of annual sighting records of plant species, we studied the correlates of local extinction risk associated with a risk of species extinction in the Park Grass Experiment where plants received long-term exposure to nutrient enrichment, soil acidification, and reductions in habitat size. We used multivariate linear models to assess how extrinsic threats and life history traits influence extinction risk. We investigated effects of four extrinsic threats (nitrogen enrichment, productivity, acidification, and plot size) as well as 11 life history traits (month of earliest flowering, flowering duration, stress tolerance, ruderalness [plant species' ability to cope with habitat disturbance], plant height, diaspore mass, seed bank, life form, dispersal mode, apomixis [the ability for a species to reproduce asexuall through seeds], and mating system). Extinction risk was not influenced by plant family. All of the 11 life history traits except life form and all threat variables influenced extinction risk but always via interactions which typically involved one threat variable and one life history trait. We detected comparatively few significant interactions between life history traits, and the interacting traits compensated for each other. These results suggest that simple predictions about extinction risk based on species' traits alone will often fail. In contrast, understanding the interactions between extrinsic threats and life history traits will allow us to make more accurate predictions of extinctions.     

Nest defence by song sparrows: methodological and life history considerations

Summary Several aspects of nest defence behavior were investigated in song sparrows (Melospiza melodia) in eastern Ontario. Two independent tests were made of the hypothesis that the increase in nest defence observed through a nesting attempt is due to the birds becoming familiar with the nest threat, rather than because the nest contents increase in value to the parents. Neither test supported the hypothesis. As predicted by life history theory for species with age-independent mortality, males did not defend their nest more vigorously as they become older. Parents defended their nests less vigorously through the breeding season, contrary to the expected pattern of increased nest defence in response to declining renesting potential. This result may be attributable to a decline in offspring value through the breeding season. Nest defence behavior of mated individuals was positively correlated, independent of factors such as offspring age, renesting potential and brood size. From this result it is proposed that a source of variation in nest defence behavior may be individuals basing their own response on their mate's response in a positive feedback fashion. Males defended nests less vigorously than females, consistent with the expectation that males have lower certainty of parentage in the offspring. It is proposed that variation in paternal uncertainty could contribute to the unexplained variation reported in nest defence studies.