Is sociality required for the evolution of communicative complexity? Evidence weighed against alternative hypotheses in diverse taxonomic groups

Complex social communication is expected to evolve whenever animals engage in many and varied social interactions; that is, sociality should promote communicative complexity. Yet, informal comparisons among phylogenetically independent taxonomic groups seem to cast doubt on the putative role of social factors in the evolution of complex communication. Here, we provide a formal test of the sociality hypothesis alongside alternative explanations for the evolution of communicative complexity. We compiled data documenting variations in signal complexity among closely related species for several case study groups--ants, frogs, lizards and birds--and used new phylogenetic methods to investigate the factors underlying communication evolution. Social factors were only implicated in the evolution of complex visual signals in lizards. Ecology, and to some degree allometry, were most likely explanations for complexity in the vocal signals of frogs (ecology) and birds (ecology and allometry). There was some evidence for adaptive evolution in the pheromone complexity of ants, although no compelling selection pressure was identified. For most taxa, phylogenetic null models were consistently ranked above adaptive models and, for some taxa, signal complexity seems to have accumulated in species via incremental or random changes over long periods of evolutionary time. Becoming social presumably leads to the origin of social communication in animals, but its subsequent influence on the trajectory of signal evolution has been neither clear-cut nor general among taxonomic groups.     

Does fecundity drive the evolution of insect diet?

We investigate whether egg load (a surrogate for fecundity) drives host specificity in a herbivorous insect. In many insects, including our study organism (Edith's checkerspot butterfly), both egg load and tendency to accept low-ranked hosts increase during each search for an oviposition site. Effects on host acceptance of egg load and passage of time are thereby potentially confounded. We conducted two experiments designed to disentangle these effects. In both experiments, we estimated the times of first acceptance of both a high-ranked and a low-ranked host, without allowing the insects to oviposit. In the first experiment, we measured egg load at the time of first acceptance of the low-ranked host. The later the time of first acceptance, the higher was the fecundity. We therefore reject the hypothesis that all insects accepted the low-ranked host at the same predetermined egg load. In the second experiment, we measured egg load 48 h after the high-ranked host was first accepted. We found no relationship between egg load and timing of acceptance of the low-ranked host. Insects with higher rates of egg accumulation did not accept the low-ranked host sooner. Taken together, these results suggest that acceptance of the low-ranked host is not driven directly by egg load. Rather, this acceptance results from some other process that is influenced by time since last oviposition. We conclude that there is no evidence to support the assumption that females with high rates of egg accumulation are more likely to accept low-ranked hosts.     

Does secotioid inertia drive the evolution of false-truffles?

Secotioid inertia is a model implemented to explain the prevalence of highly derived false-truffles with no obvious connection to the Homobasidiomycetes. The model accommodates the apparent lack of epigeous sister taxa for some highly derived hypogeous lineages by assuming that gasteromycetation in some fungi leads to the extinction of their epigeous sister population. The derived state of some hypogeous lineages suggests that they arose early in the evolution of Homobasidiomycetes and that those groups were subject to conditions that favoured hypogeous lineages such that the hypogeous fruit body form became the predominant form for some lineages. The directional selection component of secotioid inertia, termed secotioid drive, led to the extinction of their epigeous sister taxon. Morphological and molecular data from Russulaceae are used to model the evolutionary stages of secotioid inertia. The resulting phylogenetic results are compared with data from the order Leucogastrales, and the genus Destuntzia. The implications of secotioid drive are discussed with reference to gasteromycete phylogenetics, evolution, and conservation. Specifically, secotioid inertia can be used to account for reversals in fruit body morphology and instability in mycorrhizal formation.     

Does social complexity lead to sex-biased dispersal in polygynous mammals? A test on ground-dwelling sciurids

Mating systems are well known to influence the dispersing sex,but the magnitude of the sex-biased dispersal has not actuallybeen measured, whereas many theoretical predictions have beenmade. In this study, we tested a new prediction about the coevolutionbetween natal dispersal and sociality from a recent evolutionarilystable strategy (ESS) approach. From a comparative approach,we showed that, in agreement with the model, the male-biaseddispersal increases with increasing level of sociality in polygynousground-dwelling sciurids. In addition, the increase in male-biaseddispersal with increasing sociality results from an increasein male dispersal rates, whereas female dispersal rates remainconstant, contrary to what is expected from the ESS model. Althoughthe mating system through the level of polygyny could act asa confounding factor, our results strengthen previous work thatstates that inbreeding avoidance plays a major role in the evolutionof dispersal for the most social mammalian species.     

Does complexity constrain organelle evolution?

The evolution of eukaryotes was punctuated by invasions of the bacteria that have evolved to mitochondria and plastids. These bacterial endosymbionts founded major eukaryotic lineages by enabling them to carry out aerobic respiration and oxygenic photosynthesis. Yet, having evolved as free-living organisms, they were at first poorly adapted organelles. Although mitochondria and plastids have integrated within the physiology of eukaryotic cells, this integration has probably been constrained by the high level of complexity of their bacterial ancestors and the inability of gradual evolutionary processes to drastically alter complex systems. Here, I review complex processes that directly involve translation of plastid mRNAs and how they could constrain transfer to the nucleus of the genes encoding them.     

Sexual selection and intelligence: Does sexual reproduction drive the evolution of intelligence?

The basal hypothesis discussed here is the idea that brain architecture could be plastic on a very basal, genetic level due to sexual recombination and reassortment of alleles of genes related to brain development, e.g., neuronal cell adhesion molecules (NCAMs) and others.The role of sexual reassortment leads the study of brain development, species behavior and intelligence to a new version of the so-called “Red Queen Hypothesis”: using the mechanism described here, a kind of runaway selection mechanism seems to arise. Even if NCAMs are almost constant within an individual, they seem to act very differently at the population level and so the role of reassorting polymorphic NCAM- (and other) genes gets particularly clear. If several NCAM-NCAM combinations cause extreme behavior and intelligence variability in a population, these combinations also represent a use of sexual selection. This mechanism of NCAM allele assortment seems to be important for the process of speciation by mutual selection of individuals. Therefore NCAM variants and their associated behaviors are thought to be important for the development of intelligence, in that they promote the attraction of individuals with already high intelligence, leading to the speciation of super-intelligent groups.     

Does the sociality of pollinators shape the organisation of pollination networks?

A striking structural pattern of pollination networks is the presence of a few highly connected species which has implications for ecological and evolutionary processes that create and maintain diversity. To understand the structure and dynamics of pollination networks we need to know which mechanisms allow the emergence of highly connected species. We investigate whether social pollinator species are highly connected in pollination networks, and whether network structure is affected by the presence of high proportions of social pollinator species. Social insects are abundant, with long activity periods and, at the highest level of social organisation, specialised foraging castes. These three attributes are likely to increase the number of interactions of social species and, consequently, their role in pollination networks. We find that social species have, on average, more prominent network roles than solitary species, a possible mechanism being the individual‐rich colonies of social insects. However, when accounting for the shared evolutionary history of pollinators, sociality is only associated with highly interactive roles in Apidae. For apid bees, our structural equation analysis shows that the effect of sociality on species network roles is an indirect result of their high levels of interaction frequency. Despite the relative importance of sociality at a species‐level, an increasing proportion of social species in pollination networks did not affect overall network structure. Our results suggest that behavioural traits may shape patterns of interaction of individual species but not the network‐level organisation of species interactions. Instead, network structure appears to be determined by more general aspects of ecological systems such as interaction intimacy, patterns of niche overlap, and species abundance distributions.     

Calculated reciprocity? A comparative test with six primate species

Little evidence of calculated reciprocity has been found in non-human primates so far. In this study, we used a simple experimental set-up to test whether partners pulled a sliding table to altruistically provide food to each other in short-term interactions. We tested 46 dyads of chimpanzees, bonobos, gorillas, orangutans, brown capuchin monkeys and spider monkeys to examine whether a subject’s tendency to provide food to a partner was directly affected by the partner’s previous behaviour, by the species, by the condition (i.e., whether the partner could access the food provided by the subject) and by the social tolerance levels within each dyad. Chimpanzees and orangutans were the only species pulling significantly more when the partner could retrieve the food altruistically provided. However, no species reciprocated food exchanges, as subjects’ probability to pull was not affected by the previous number of the partner’s pulls, with the possible exception of one orangutan dyad. Although subjects clearly knew how the apparatus worked and easily obtained food for themselves, individuals did not usually take the opportunity to provide food to their partners, suggesting that calculated reciprocity is not a common behaviour and that food exchanges are usually not reciprocated in the short-term within dyads.     

Does morphological convergence imply functional similarity? A test using the evolution of quadrupedalism in ornithischian dinosaurs

Convergent morphologies are thought to indicate functional similarity, arising because of a limited number of evolutionary or developmental pathways. Extant taxa displaying convergent morphologies are used as analogues to assess function in extinct taxa with similar characteristics. However, functional studies of extant taxa have shown that functional similarity can arise from differing morphologies, calling into question the paradigm that form and function are closely related. We test the hypothesis that convergent skeletal morphology indicates functional similarity in the fossil record using ornithischian dinosaurs. The rare transition from bipedality to quadrupedality occurred at least three times independently in this clade, resulting in a suite of convergent osteological characteristics. We use homology rather than analogy to provide an independent line of evidence about function, reconstructing soft tissues using the extant phylogenetic bracket and applying biomechanical concepts to produce qualitative assessments of muscle leverage. We also optimize character changes to investigate the sequence of character acquisition. Different lineages of quadrupedal ornithischian dinosaur stood and walked differently from each other, falsifying the hypothesis that osteological convergence indicates functional similarity. The acquisition of features correlated with quadrupedalism generally occurs in the same order in each clade, suggesting underlying developmental mechanisms that act as evolutionary constraints.     

Does constructive neutral evolution play an important role in the origin of cellular complexity?

Recently, constructive neutral evolution has been touted as an important concept for the understanding of the emergence of cellular complexity. It has been invoked to help explain the development and retention of, amongst others, RNA splicing, RNA editing and ribosomal and mitochondrial respiratory chain complexity. The theory originated as a welcome explanation of isolated small scale cellular idiosyncrasies and as a reaction to 'overselectionism'. Here I contend, that in its extended form, it has major conceptual problems, can not explain observed patterns of complex processes, is too easily dismissive of alternative selectionist models, underestimates the creative force of complexity as such, and--if seen as a major evolutionary mechanism for all organisms--could stifle further thought regarding the evolution of highly complex biological processes.     

Does intraspecific hybridization contribute to the evolution of invasiveness?: an experimental test

One of the major objectives of research on invasive species is to determine the relative importance of different evolutionary and ecological forces in the invasion process. It was recently suggested that post-introduction intraspecific hybridization between previously isolated genotypes could produce novel and/or heterotic progeny that might express enhanced invasiveness. We tested this hypothesis with Silene latifolia, a European native that has successfully invaded North America and has previously been shown to have undergone genetic change since its introduction. In a common garden experiment we compared the performance of plants derived from within and between population crosses from eight European and 18 North American populations. Results showed that there was no significant effect of crossing distance on progeny phenotype. Furthermore, progeny from within or between population crosses did not differ in size, reproductive output or survival. Collectively, these results suggest that the invasive phenotype of S. latifolia is likely the result of natural selection and/or genetic drift rather than intraspecific hybridization.     

Philopatric reproduction, a prime mover in the evolution of termite sociality?

Summary: Philopatric reproduction commonly occurs even in the most basic isopteran lineages and is almost certainly a primitive potentiality of these insects. Several authors hypothesized that opportunities for philopatric reproduction may have been a prime mover for the three most remarkable events in the evolution of termite sociality: the origin of helping behaviour, the origin of soldiers, and the origin of a permanently apterous worker caste. A critical assessment of these hypotheses and a review of relevant evidence are presented here. I first discuss the hypothesis that termite helpers derive from individuals choosing to postpone dispersal because of nest inheritance prospects. Such individuals would have developed helping as a strategy yielding indirect reproductive benefits while they wait for reproductive opportunities. However, it appears that prospects of philopatric reproduction need not be invoked to explain the origin of helping behaviour, which can be justified more parsimoniously by a favourable intrinsic benefit/cost ratio. Second, the hypothesis that soldiers originated through selection for fighting abilities among neotenic reproductives is found to face important difficulties, the major one being how to explain the absence of fighting devices in almost all present-day neotenics. Finally, the hypothesized link between apterism and chances of philopatric reproduction, which might have favoured the onset of the worker caste, is poorly supported by empirical evidence. It appears thus that philopatric reproduction, notwithstanding its importance in the biology of many extant termite species, is unlikely to have been a prime mover in the evolution of helping and of altruistic castes in termites.     

Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes

Background  

One of the main explanations for the stunning diversity of teleost fishes (~29,000 species, nearly half of all vertebrates) is that a fish-specific whole-genome duplication event (FSGD) in the ancestor to teleosts triggered their subsequent radiation. However, one critical assumption of this hypothesis, that diversification rates in teleosts increased soon after the acquisition of a duplicated genome, has never been tested.