Ecology and evolution of social-organization: insights from fire ants and other highly eusocial insects

Social organisms exhibit conspicuous intraspecific variation in all facets of their social organization. A prominent example of such variation in the highly eusocial Hymenoptera is differences in the number of reproductive queens per colony, Differences in queen number in ants are associated with differences in a host of reproductive and social traits, including queen phenotype and breeding strategy, mode of colony reproduction, and pattern of sex allocation. We examine the causes and consequences of changes in colony queen number and associated traits using the fire ant Solenopsis invicta as a principal model. Ecological constraints on mode of colony founding may act as important selective forces causing the evolution of queen number in this and many other ants, with social organization generally perpetuated across generations by means of the social environment molding appropriate queen phenotypes and reproductive strategies. Shifts in colony queen number have profound effects on genetic structure within nests and may also influence genetic structure at higher levels (aggregations of nests or local demes) because of the association of queen number with particular mating and dispersal habits. Divergence of breeding habits between populations with different social organizations has the potential to promote genetic differentiation between these social variants. Thus, evolution of social organization can be important in generating intrinsic selective regimes that channel subsequent social evolution and in initiating the development of significant population genetic structure, including barriers to gene flow important in cladogenesis.

An evolutionary perspective on self-organized division of labor in social insects

Division of labor is a complex phenomenon observed throughout nature. Theoretical studies have focused either on its emergence through self-organization mechanisms or on its adaptive consequences. We suggest that the interaction of self-organization, which undoubtedly characterizes division of labor in social insects, and evolution should be further explored. We review the factors empirically shown to influence task choice. In light of these factors, we review the most important self-organization and evolutionary models for division of labor and outline their advantages and limitations. We describe ways to unify evolution and self-organization in the theoretical study of division of labor and recent results in this area. Finally, we discuss some benchmarks and primary challenges of this approach.

Bayesian estimation of speciation and extinction from incomplete fossil occurrence data.

The temporal dynamics of species diversity are shaped by variations in the rates of speciation and extinction, and there is a long history of inferring these rates using first and last appearances of taxa in the fossil record. Understanding diversity dynamics critically depends on unbiased estimates of the unobserved times of speciation and extinction for all lineages, but the inference of these parameters is challenging due to the complex nature of the available data. Here, we present a new probabilistic framework to jointly estimate species-specific times of speciation and extinction and the rates of the underlying birth-death process based on the fossil record. The rates are allowed to vary through time independently of each other, and the probability of preservation and sampling is explicitly incorporated in the model to estimate the true lifespan of each lineage. We implement a Bayesian algorithm to assess the presence of rate shifts by exploring alternative diversification models. Tests on a range of simulated data sets reveal the accuracy and robustness of our approach against violations of the underlying assumptions and various degrees of data incompleteness. Finally, we demonstrate the application of our method with the diversification of the mammal family Rhinocerotidae and reveal a complex history of repeated and independent temporal shifts of both speciation and extinction rates, leading to the expansion and subsequent decline of the group. The estimated parameters of the birth-death process implemented here are directly comparable with those obtained from dated molecular phylogenies. Thus, our model represents a step towards integrating phylogenetic and fossil information to infer macroevolutionary processes.

Hydrocarbon divergence and reproductive isolation in Timema stick insects.

BACKGROUND: Individuals commonly prefer certain trait values over others when choosing their mates. If such preferences diverge between populations, they can generate behavioral reproductive isolation and thereby contribute to speciation. Reproductive isolation in insects often involves chemical communication, and cuticular hydrocarbons, in particular, serve as mate recognition signals in many species. We combined data on female cuticular hydrocarbons, interspecific mating propensity, and phylogenetics to evaluate the role of cuticular hydrocarbons in diversification of Timema walking-sticks. RESULTS: Hydrocarbon profiles differed substantially among the nine analyzed species, as well as between partially reproductively-isolated T. cristinae populations adapted to different host plants. In no-choice trials, mating was more likely between species with similar than divergent hydrocarbon profiles, even after correcting for genetic divergences. The macroevolution of hydrocarbon profiles, along a Timema species phylogeny, fits best with a punctuated model of phenotypic change concentrated around speciation events, consistent with change driven by selection during the evolution of reproductive isolation. CONCLUSION: Altogether, our data indicate that cuticular hydrocarbon profiles vary among Timema species and populations, and that most evolutionary change in hydrocarbon profiles occurs in association with speciation events. Similarities in hydrocarbon profiles between species are correlated with interspecific mating propensities, suggesting a role for cuticular hydrocarbon profiles in mate choice and speciation in the genus Timema.

Nd and Sr isotope compositions in modern and fossil bones - Proxies for vertebrate provenance and taphonomy

Rare earth elements (REE), while not essential for the physiologic functions of animals, are ingested and incorporated in ppb concentrations in bones and teeth. Nd isotope compositions of modern bones of animals from isotopically distinct habitats demonstrate that the (143)Nd/(144)Nd of the apatite can be used as a fingerprint for bedrock geology or ambient water mass. This potentially allows the provenance and migration of extant vertebrates to be traced, similar to the use of Sr isotopes. Although REE may be enriched by up to 5 orders of magnitude during diagenesis and recrystallization of bone apatite, in vivo (143)Nd/(144)Nd may be preserved in the inner cortex of fossil bones or enamel. However, tracking the provenance of ancient or extinct vertebrates is possible only for well-preserved archeological and paleontological skeletal remains with in vivo-like Nd contents at the ppb-level. Intra-bone and -tooth REE analysis can be used to screen for appropriate areas. Large intra-bone Nd concentration gradients of 10(1)-10(3) are often measured. Nd concentrations in the inner bone cortex increase over timescales of millions of years, while bone rims may be enriched over millenial timescales. Nevertheless, epsilon(Nd) values are often similar within one epsilon(Nd) unit within a single bone. Larger intra-bone differences in specimens may either reflect a partial preservation of in vivo values or changing epsilon(Nd) values of the diagenetic fluid during fossilization. However, most fossil specimens and the outer rims of bones will record taphonomic (143)Nd/(144)Nd incorporated post mortem during diagenesis. Unlike REE patterns, (143)Nd/(144)Nd are not biased by fractionation processes during REE-uptake into the apatite crystal lattice, hence the epsilon(Nd) value is an important tracer for taphonomy and reworking. Bones and teeth from autochthonous fossil assemblages have small variations of +/- 1 epsilon(Nd) unit only. In contrast, fossil bones and teeth from over 20 different marine and terrestrial fossil sites have a total range of epsilon(Nd) values from -13.0 to 4.9 (n = 80), often matching the composition of the embedding sediment. This implies that the surrounding sediment is the source of Nd in the fossil bones and that the specimens of this study seem not to have been reworked. Differences in epsilon(Nd) values between skeletal remains and embedding sediment may either indicate reworking of fossils and/or a REE-uptake from a diagenetic fluid with non-sediment derived epsilon(Nd) values. The latter often applies to fossil shark teeth, which may preserve paleo-seawater values. Complementary to epsilon(Nd) values, (87)Sr/(86)Sr can help to further constrain the fossil provenance and reworking. (C) 2011 Elsevier Ltd. All rights reserved.

Insights from insects about adaptive social information use.

Copying others can greatly improve individual fitness and is fundamental for the organisation of societies. Yet in some situations it is better to ignore social information and either explore the world individually or use personal information obtained through prior experience. Insects provide excellent models to study the strategic use of social information, but insights from recent research have rarely been viewed in the light of social learning strategies. Here we discuss how insects tailor their reliance on social information to those circumstances for which it is most beneficial, and suggest that insects and vertebrates use similar information-use strategies. We highlight future research avenues, including the use of molecular tools to study the genetic and genomic basis of social information use.

Neutral and selection-driven decay of sexual traits in asexual stick insects.

Environmental shifts and lifestyle changes may result in formerly adaptive traits becoming non-functional or maladaptive. The subsequent decay of such traits highlights the importance of natural selection for adaptations, yet its causes have rarely been investigated. To study the fate of formerly adaptive traits after lifestyle changes, we evaluated sexual traits in five independently derived asexual lineages, including traits that are specific to males and therefore not exposed to selection. At least four of the asexual lineages retained the capacity to produce males that display normal courtship behaviours and are able to fertilize eggs of females from related sexual species. The maintenance of male traits may stem from pleiotropy, or from these traits only regressing via drift, which may require millions of years to generate phenotypic effects. By contrast, we found parallel decay of sexual traits in females. Asexual females produced altered airborne and contact signals, had modified sperm storage organs, and lost the ability to fertilize their eggs, impeding reversals to sexual reproduction. Female sexual traits were decayed even in recently derived asexuals, suggesting that trait changes following the evolution of asexuality, when they occur, proceed rapidly and are driven by selective processes rather than drift.

The assessment of reproductive success of queens in ants and other social insects

Recently considerable research has focused on the causes of evolution of multiple-queen (polygynous) colonies. In order to better understand the factors which may have led to these polygynous associations it is vital to compare the reproductive success of queens in monogynous (one queen per colony) and polygynous colonies as well as the relative fitness of queens in polygynous colonies. This paper addresses the difficulties arising from such comparisons and their implications with regard to the methods commonly used to assess reproductive success in queens. The relative reproductive success of queens in monogynous and polygynous colonies is commonly assessed by comparing the relative number of reproductives they produce during a single reproductive season. However, shift in queen number seems to be only one aspect of a profound shift in social structure and reproductive strategy that constitutes, in effect, a ''polygyny syndrome''. For example, female reproductives produced in polygynous colonies frequently use a different mode of colony founding, which in turn affects the probability of their survival. Furthermore, queens from monogynous and polygynous colonies frequently differ in their life-span and the number of sexual broods they produce. As a result, the reproductive success of queens in monogynous and polygynous colonies may not be directly related to the relative number of sexuals they produce during a single reproductive season.

Molecular evidence for ancient asexuality in timema stick insects.

Asexuality is rare in animals in spite of its apparent advantage relative to sexual reproduction, indicating that it must be associated with profound costs [1-9]. One expectation is that reproductive advantages gained by new asexual lineages will be quickly eroded over time [3, 5-7]. Ancient asexual taxa that have evolved and adapted without sex would be "scandalous" exceptions to this rule, but it is often difficult to exclude the possibility that putative asexuals deploy some form of "cryptic" sex, or have abandoned sex more recently than estimated from divergence times to sexual relatives [10]. Here we provide evidence, from high intraspecific divergence of mitochondrial sequence and nuclear allele divergence patterns, that several independently derived Timema stick-insect lineages have persisted without recombination for more than a million generations. Nuclear alleles in the asexual lineages displayed significantly higher intraindividual divergences than in related sexual species. In addition, within two asexuals, nuclear allele phylogenies suggested the presence of two clades, with sequences from the same individual appearing in both clades. These data strongly support ancient asexuality in Timema and validate the genus as an exceptional opportunity to attack the question of how asexual reproduction can be maintained over long periods of evolutionary time.

Population genomics of eusocial insects: the costs of a vertebrate-like effective population size

The evolution of reproductive division of labour and social life in social insects has lead to the emergence of several life-history traits and adaptations typical of larger organisms: social insect colonies can reach masses of several kilograms, they start reproducing only when they are several years old, and can live for decades. These features and the monopolization of reproduction by only one or few individuals in a colony should affect molecular evolution by reducing the effective population size. We tested this prediction by analysing genome-wide patterns of coding sequence polymorphism and divergence in eusocial vs. noneusocial insects based on newly generated RNA-seq data. We report very low amounts of genetic polymorphism and an elevated ratio of nonsynonymous to synonymous changes - a marker of the effective population size - in four distinct species of eusocial insects, which were more similar to vertebrates than to solitary insects regarding molecular evolutionary processes. Moreover, the ratio of nonsynonymous to synonymous substitutions was positively correlated with the level of social complexity across ant species. These results are fully consistent with the hypothesis of a reduced effective population size and an increased genetic load in eusocial insects, indicating that the evolution of social life has important consequences at both the genomic and population levels.

Long live the queen: studying aging in social insects

Aging is a fascinating, albeit controversial, chapter in biology. Few other subjects have elicited more than a century of ever-increasing scientific interest. In this review, we discuss studies on aging in social insects, a group of species that includes ants and termites, as well as certain bee and wasp species. One striking feature of social insects is the lifespan of queens (reproductive females), which can reach nearly 30 years in some ant species. This is over 100 times the average lifespan of solitary insects. Moreover, there is a tremendous variation in lifespan among castes, with queens living up to 500 times longer than males and 10 times longer than workers (non-reproductive individuals). This lifespan polymorphism has allowed researchers to test the evolutionary theory of aging and Y more recently Y to investigate the proximate causes of aging. The originality of these studies lies in their use of naturally evolved systems to address questions related to aging and lifespan determination that cannot be answered using the conventional model organisms.

Female stick insects mate multiply to find compatible mates

Why females of many species mate multiply in the absence of direct benefits remains an open question in evolutionary ecology. Interacting and mating with multiple males can be costly to females in terms of time, resources, predation risk, and disease transmission. A number of indirect genetic benefits have been proposed to explain such behaviors, but the relative importance of these mechanisms in natural systems remains unclear. We tested for several direct and indirect benefits of polyandry in the walking stick Timema cristinae. We found no evidence of direct benefits with respect to longevity or fecundity. However, male x female genotypic interactions affected egg-hatching success and offspring production independent of relatedness, suggesting that mating with certain males benefits females and that the best male may differ for each female. Furthermore, multiply mated females biased paternity toward one or few males, and the extent of this bias was positively correlated to egg-hatching success. Our data, therefore, provide evidence for indirect benefits through compatibility effects in this species. By mating multiply, females may improve their chances of mating with a compatible male if compatibility cannot be assessed before mating. Such compatibility effects can explain the evolution and maintenance of polyandry in Timema and many other species.