Biogeography and evolution of social parasitism in Australian Myrmecia bulldog ants revealed by phylogenomics.

Studying the historical biogeography and life history transitions from eusocial colony life to social parasitism contributes to our understanding of the evolutionary mechanisms generating biodiversity in eusocial insects. The ants in the genus Myrmecia are a well-suited system for testing evolutionary hypotheses about how their species diversity was assembled through time because the genus is endemic to Australia with the single exception of the species M. apicalis inhabiting the Pacific Island of New Caledonia, and because at least one social parasite species exists in the genus. However, the evolutionary mechanisms underlying the disjunct biogeographic distribution of M. apicalis and the life history transition(s) to social parasitism remain unexplored. To study the biogeographic origin of the isolated, oceanic species M. apicalis and to reveal the origin and evolution of social parasitism in the genus, we reconstructed a comprehensive phylogeny of the ant subfamily Myrmeciinae. We utilized Ultra Conserved Elements (UCEs) as molecular markers to generate a molecular genetic dataset consisting of 2,287 loci per taxon on average for 66 out of the 93 known Myrmecia species as well as for the sister lineage Nothomyrmecia macrops and selected outgroups. Our time-calibrated phylogeny inferred that: (i) stem Myrmeciinae originated during the Paleocene âˆ¼ 58 Ma ago; (ii) the current disjunct biogeographic distribution of M. apicalis was driven by long-distance dispersal from Australia to New Caledonia during the Miocene âˆ¼ 14 Ma ago; (iii) the single social parasite species, M. inquilina, evolved directly from one of the two known host species, M. nigriceps, in sympatry via the intraspecific route of social parasite evolution; and (iv) 5 of the 9 previously established taxonomic species groups are non-monophyletic. We suggest minor changes to reconcile the molecular phylogenetic results with the taxonomic classification. Our study enhances our understanding of the evolution and biogeography of Australian bulldog ants, contributes to our knowledge about the evolution of social parasitism in ants, and provides a solid phylogenetic foundation for future inquiries into the biology, taxonomy, and classification of Myrmeciinae.

The general form of Hamilton's rule makes no predictions and cannot be tested empirically.

Hamilton's rule asserts that a trait is favored by natural selection if the benefit to others, [Formula: see text], multiplied by relatedness, [Formula: see text], exceeds the cost to self, [Formula: see text] Specifically, Hamilton's rule states that the change in average trait value in a population is proportional to [Formula: see text] This rule is commonly believed to be a natural law making important predictions in biology, and its influence has spread from evolutionary biology to other fields including the social sciences. Whereas many feel that Hamilton's rule provides valuable intuition, there is disagreement even among experts as to how the quantities [Formula: see text], [Formula: see text], and [Formula: see text] should be defined for a given system. Here, we investigate a widely endorsed formulation of Hamilton's rule, which is said to be as general as natural selection itself. We show that, in this formulation, Hamilton's rule does not make predictions and cannot be tested empirically. It turns out that the parameters [Formula: see text] and [Formula: see text] depend on the change in average trait value and therefore cannot predict that change. In this formulation, which has been called "exact and general" by its proponents, Hamilton's rule can "predict" only the data that have already been given.

An ant genus-group (Prenolepis) illuminates the biogeography and drivers of insect diversification in the Indo-Pacific.

The Malay Archipelago and the tropical South Pacific (hereafter the Indo-Pacific region) are considered biodiversity hotspots, yet a general understanding of the origins and diversification of species-rich groups in the region remains elusive. We aimed to test hypotheses for the evolutionary processes driving insect species diversity in the Indo-Pacific using a higher-level and comprehensive phylogenetic hypothesis for an ant clade consisting of seven genera. We estimated divergence times and reconstructed the biogeographical history of ant species in the Prenolepis genus-group (Formicidae: Formicinae: Lasiini). We used a fossil-calibrated phylogeny to infer ancestral geographical ranges utilizing a biogeographic model that includes founder-event speciation. Ancestral state reconstructions of the ants' ecological preferences, and diversification rates were estimated for selected Indo-Pacific clades. Overall, we report that faunal interchange between Asia and Australia has occurred since at least 20-25 Ma, and early dispersal to the Fijian Basin happened during the early and mid-Miocene (ca. 10-20 Ma). Differences in diversification rates across Indo-Pacific clades may be related to ecological preference breadth, which in turn may have facilitated geographical range expansions. Ancient dispersal routes suggested by our results agree with the palaeogeography of the region. For this particular group of ants, the rapid orogenesis in New Guinea and possibly subsequent ecological shifts may have promoted their rapid diversification and widespread distribution across the Indo-Pacific.

Natural selection drives the evolution of ant life cycles.

The genetic origin of advanced social organization has long been one of the outstanding problems of evolutionary biology. Here we present an analysis of the major steps in ant evolution, based for the first time, to our knowledge, on combined recent advances in paleontology, phylogeny, and the study of contemporary life histories. We provide evidence of the causal forces of natural selection shaping several key phenomena: (i) the relative lateness and rarity in geological time of the emergence of eusociality in ants and other animal phylads; (ii) the prevalence of monogamy at the time of evolutionary origin; and (iii) the female-biased sex allocation observed in many ant species. We argue that a clear understanding of the evolution of social insects can emerge if, in addition to relatedness-based arguments, we take into account key factors of natural history and study how natural selection acts on alleles that modify social behavior.

The evolution of eusociality.

Eusociality, in which some individuals reduce their own lifetime reproductive potential to raise the offspring of others, underlies the most advanced forms of social organization and the ecologically dominant role of social insects and humans. For the past four decades kin selection theory, based on the concept of inclusive fitness, has been the major theoretical attempt to explain the evolution of eusociality. Here we show the limitations of this approach. We argue that standard natural selection theory in the context of precise models of population structure represents a simpler and superior approach, allows the evaluation of multiple competing hypotheses, and provides an exact framework for interpreting empirical observations.

Limitations of inclusive fitness.

Until recently, inclusive fitness has been widely accepted as a general method to explain the evolution of social behavior. Affirming and expanding earlier criticism, we demonstrate that inclusive fitness is instead a limited concept, which exists only for a small subset of evolutionary processes. Inclusive fitness assumes that personal fitness is the sum of additive components caused by individual actions. This assumption does not hold for the majority of evolutionary processes or scenarios. To sidestep this limitation, inclusive fitness theorists have proposed a method using linear regression. On the basis of this method, it is claimed that inclusive fitness theory (i) predicts the direction of allele frequency changes, (ii) reveals the reasons for these changes, (iii) is as general as natural selection, and (iv) provides a universal design principle for evolution. In this paper we evaluate these claims, and show that all of them are unfounded. If the objective is to analyze whether mutations that modify social behavior are favored or opposed by natural selection, then no aspect of inclusive fitness theory is needed.

Molecular phylogeny of Indo-Pacific carpenter ants (Hymenoptera: Formicidae, Camponotus) reveals waves of dispersal and colonization from diverse source areas.

Ants that resemble Camponotus maculatus (Fabricius, 1782) present an opportunity to test the hypothesis that the origin of the Pacific island fauna was primarily New Guinea, the Philippines, and the Indo-Malay archipelago (collectively known as Malesia). We sequenced two mitochondrial and four nuclear markers from 146 specimens from Pacific islands, Australia, and Malesia. We also added 211 specimens representing a larger worldwide sample and performed a series of phylogenetic analyses and ancestral area reconstructions. Results indicate that the Pacific members of this group comprise several robust clades that have distinctly different biogeographical histories, and they suggest an important role for Australia as a source of Pacific colonizations. Malesian areas were recovered mostly in derived positions, and one lineage appears to be Neotropical. Phylogenetic hypotheses indicate that the orange, pan-Pacific form commonly identified as C. chloroticus Emery 1897 actually consists of two distantly related lineages. Also, the lineage on Hawai'i, which has been called C. variegatus (Smith, 1858), appears to be closely related to C. tortuganus Emery, 1895 in Florida and other lineages in the New World. In Micronesia and Polynesia the C. chloroticus-like species support predictions of the taxon-cycle hypothesis and could be candidates for human-mediated dispersal.

Environment: early ant plagues in the New World.

The identity and origin of the West Indian plague ants of the early sixteenth and late eighteenth centuries have long been a mystery. By reviewing historic accounts with an analysis of the present-day Caribbean ant fauna, I have narrowed the list of suspects to two species and their insect symbionts.

Breaking out of biogeographical modules: range expansion and taxon cycles in the hyperdiverse ant genus Pheidole.

AIM: We sought to reconstruct the biogeographical structure and dynamics of a hyperdiverse ant genus, Pheidole, and to test several predictions of the taxon cycle hypothesis. Using large datasets on Pheidole geographical distributions and phylogeny, we (1) inferred patterns of biogeographical modularity (clusters of areas with similar faunal composition), (2) tested whether species in open habitats are more likely to be expanding their range beyond module boundaries, and (3) tested whether there is a bias of lineage flow from high- to low-diversity areas. LOCATION: The Old World. METHODS: We compiled and jointly analysed a comprehensive database of Pheidole geographical distributions, the ecological affinities of different species, and a multilocus phylogeny of the Old World radiation. We used network modularity methods to infer biogeographical structure in the genus and comparative methods to evaluate the hypotheses. RESULTS: The network analysis identified eight biogeographical modules, and a suite of species with anomalous ranges that are statistically more likely to occur in open habitat, supporting the hypothesis that open habitats promote range expansion. Phylogenetic analysis shows evidence for a cascade pattern of colonization from Asia to New Guinea to the Pacific, but no 'upstream' colonization in the reverse direction. MAIN CONCLUSIONS: The distributions of Pheidole lineages in the Old World are highly modular, with modules generally corresponding to biogeographical regions inferred in other groups of organisms. However, some lineages have expanded their ranges across module boundaries, and these species are more likely to be adapted to open habitats rather than interior forest. In addition, there is a cascade pattern of dispersal from higher to lower diversity areas during these range expansions. Our findings are consistent with the taxon cycle hypothesis, although they do not rule out alternative interpretations.

Social insect histology from the nineteenth century: the magnificent pioneer sections of Charles Janet.

Charles Janet (1849-1932) was the leading pioneer in the histological description of the internal anatomy of social insects, in particular of ants and wasps. Because many of the original Janet sections still exist, this article is able to illustrate the amazing skills through some selected pictures taken from this more than a century old material, and thus to pay tribute to this French founder of insect morphology.

Rethinking the theoretical foundation of sociobiology.

Current sociobiology is in theoretical disarray, with a diversity of frameworks that are poorly related to each other Part of the problem is a reluctance to revisit the pivotal events that took place during the 1960s, including the rejection of group selection and the development of alternative theoretical frameworks to explain the evolution of cooperative and altruistic behaviors. In this article, we take a "back to basics" approach, explaining what group selection is, why its rejection was regarded as so important, and how it has been revived based on a more careful formulation and subsequent research. Multilevel selection theory (including group selection) provides an elegant theoretical foundation for sociobiology in the future, once its turbulent past is appropriately understood.

The rise of the ants: a phylogenetic and ecological explanation.

In the past two decades, studies of anatomy, behavior, and, most recently, DNA sequences have clarified the phylogeny of the ants at the subfamily and generic levels. In addition, a rich new harvest of Cretaceous and Paleogene fossils has helped to date the major evolutionary radiations. We collate this information and then add data from the natural history of the modern fauna to sketch a history of major ecological adaptations at the subfamily level. The key events appear to have been, first, a mid-Cretaceous initial radiation in forest ground litter and soil coincident with the rise of the angiosperms (flowering plants), then a Paleogene advance to ecological dominance in concert with that of the angiosperms in tropical forests, and, finally, an expansion of some of the lineages, aided by changes in diet away from dependence on predation, upward into the canopy, and outward into more xeric environments.

Eusociality: origin and consequences.

In this new assessment of the empirical evidence, an alternative to the standard model is proposed: group selection is the strong binding force in eusocial evolution; individual selection, the strong dissolutive force; and kin selection (narrowly defined), either a weak binding or weak dissolutive force, according to circumstance. Close kinship may be more a consequence of eusociality than a factor promoting its origin. A point of no return to the solitary state exists, as a rule when workers become anatomically differentiated. Eusociality has been rare in evolution, evidently due to the scarcity of environmental pressures adequate to tip the balance among countervailing forces in favor of group selection. Eusociality in ants and termites in the irreversible stage is the key to their ecological dominance and has (at least in ants) shaped some features of internal phylogeny. Their colonies are consistently superior to solitary and preeusocial competitors, due to the altruistic behavior among nestmates and their ability to organize coordinated action by pheromonal communication.