Identifying Causes of Social Evolution: Contextual Analysis, the Price Approach, and Multilevel Selection

Kin selection theory and multilevel selection theory are distinct approaches to explaining the evolution of social traits. The latter claims that it is useful to regard selection as a process that can occur on multiple levels of organisation such as the level of individuals and the level of groups. This is reflected in a decomposition of fitness into an individual component and a group component. This multilevel view is central to understanding and characterising evolutionary transitions in individuality, e.g., from unicellular life to multicellular organisms, but currently suffers from the lack of a consistent, quantifiable measure. Specifically, the two major statistical tools to determine the coefficients of such a decomposition, the multilevel Price equation and contextual analysis, are inconsistent and may disagree on whether group selection is present. Here we show that the reason for the discrepancies is that underlying the multilevel Price equation and contextual analysis are two non-equivalent causal models for the generation of individual fitness effects (thus leaving different “remainders” explained by group effects). While the multilevel Price equation assumes that the individual effect of a trait determines an individual's relative success within a group, contextual analysis posits that the individual effect is context-independent. Since these different assumptions reflect claims about the causal structure of the system, the correct approach cannot be determined on general theoretical or statistical grounds but must be identified by experimental intervention. We outline interventions that reveal the underlying causal structure and thus facilitate choosing the appropriate approach. We note that kin selection theory with its focus on the individual is immune to such inconsistency because it does not address causal structure with respect to levels of organisation. In contrast, our analysis of the two approaches to measuring group selection demonstrates that multilevel selection theory adds meaningful (falsifiable) causal structure to explain the sources of individual fitness and thereby constitutes a proper refinement of kin selection theory. Taking such refined causal structure into account seems indispensable for studying evolutionary transitions in individuality because these transitions are characterised by changes in the selection pressures that act on the respective levels.

Major Evolutionary Transitions and the Roles of Facilitation and Information in Ecosystem Transformations

A small number of extraordinary “Major Evolutionary Transitions” (METs) have attracted attention among biologists. They comprise novel forms of individuality and information, and are defined in relation to organismal complexity, irrespective of broader ecosystem-level effects. This divorce between evolutionary and ecological consequences qualifies unicellular eukaryotes, for example, as a MET although they alone failed to significantly alter ecosystems. Additionally, this definition excludes revolutionary innovations not fitting into either MET type (e.g., photosynthesis). We recombine evolution with ecology to explore how and why entire ecosystems were newly created or radically altered – as Major System Transitions (MSTs). In doing so, we highlight important morphological adaptations that spread through populations because of their immediate, direct-fitness advantages for individuals. These are Major Competitive Transitions, or MCTs. We argue that often multiple METs and MCTs must be present to produce MSTs. For example, sexually-reproducing, multicellular eukaryotes (METs) with anisogamy and exoskeletons (MCTs) significantly altered ecosystems during the Cambrian. Therefore, we introduce the concepts of Facilitating Evolutionary Transitions (FETs) and Catalysts as key events or agents that are insufficient themselves to set a MST into motion, but are essential parts of synergies that do. We further elucidate the role of information in MSTs as transitions across five levels: (I) Encoded; (II) Epigenomic; (III) Learned; (IV) Inscribed; and (V) Dark Information. The latter is ‘authored’ by abiotic entities rather than biological organisms. Level IV has arguably allowed humans to produce a MST, and V perhaps makes us a FET for a future transition that melds biotic and abiotic life into one entity. Understanding the interactive processes involved in past major transitions will illuminate both current events and the surprising possibilities that abiotically-created information may produce.

Conspicuous female plumage is common among open cup-nesting passerine birds

Alfred Russel Wallace hypothesized that the use of cavity or dome nests releases incubating birds from predation risk, and that this allows the evolution of conspicuous coloration in females. By this hypothesis, females that use open nests are subject to strong selection for crypsis. Here, we test the validity of Wallace’s proposed evolutionary correlation between nest type and conspicuous coloration in females across the largest avian radiation, the Passeriformes, using phylogenetic comparative methods. We also test an alternate hypothesis that cavity-nesting results in greater conspicuousness because competition for cavities is stronger than for other nest sites, and such competition can drive social selection on female plumage. By this hypothesis, dome-nesting females should generally be less conspicuous than cavity-nesting species. We found no support for Wallace’s hypothesis that concealed nests yield conspicuous plumage while open nests yield dull plumage, and some support for the social selection hypothesis in smaller-bodied, gregarious species. While our analyses do not support the core part of Wallace’s hypothesis, they corroborate his contention that evolutionary transitions in nest type are rare, indicating that nest types may influence macroevolutionary selective regimes for other traits.

Is chiropterophily an evolutionary dead end? A phylogenetic test in the pantropical genus Parkia (Leguminosae, Caesalpinioideae, mimosoid clade)

Background and aims – Pollination systems often reflect adaptations to specific groups of pollinators, and these morphological specialisations have been important in the diversification of the angiosperms. Here, we study the evolution of the capitulum and pollination system in the pantropical genus Parkia, which comprises 35 species of trees distributed largely in the forests of South and Central America, Africa, Madagascar, and the Indo-Pacific. The flowers are grouped into capitula that are composed of one, two, or three distinct morphological types, and are principally pollinated either by insects or by bats. Material and methods – Using BEAST, we estimated the ages of nodes in a phylogeny based on four chloroplast regions (matK, trnL, psbA-trnH, and rps16-trnQ) and the nuclear region ITS/18S/26S. This analysis also enabled us to reconstruct the ancestral state of the capitulum and hence infer the ancestral pollination system. Euclidean distance-based cluster analysis was performed to determine which characters are consistently related to a specific pollination system.Key results – Our results indicate that the ancestral capitulum in the genus had three types of flowers and a morphology associated with bat-pollination in both the Paleotropics and Neotropics. In one derived Neotropical clade, the number of floral types in each capitulum was reduced to two (capitulum also bat-pollinated) or one (insect-pollinated). Thus, entomophily, as seen in some Neotropical species of Parkia, has been derived from a bat-pollinated ancestor. Cluster analysis showed that the floral characters were mostly consistent with pollination systems.Conclusion – Chiropterophily is not an evolutionary dead end in Parkia because during the evolutionary history of the genus there has been at least one transition to entomophily. Parkia provides a unique example of evolutionary transitions from chiropterophily to entomophily in a pantropical genus of trees.

Major Evolutionary Transitions in Social Insects, the Importance of Worker Sterility and Life History Trade-Offs

The evolution of eusociality in social insects, such as termites, ants, and some bees and wasps, has been regarded as a major evolutionary transition (MET). Yet, there is some debate whether all species qualify. Here, we argue that worker sterility is a decisive criterion to determine whether species have passed a MET (= superorganisms), or not. When workers are sterile, reproductive interests align among group members as individual fitness is transferred to the colony level. Division of labour among cooperating units is a major driver that favours the evolution of METs across all biological scales. Many METs are characterised by a differentiation into reproductive versus maintenance functions. In social insects, the queen specialises on reproduction while workers take over maintenance functions such as food provisioning. Such division of labour allows specialisation and it reshapes life history trade-offs among cooperating units. For instance, individuals within colonies of social insects can overcome the omnipresent fecundity/longevity trade-off, which limits reproductive success in organisms, when increased fecundity shortens lifespan. Social insect queens (particularly in superorganismal species) can reach adult lifespans of several decades and are among the most fecund terrestrial animals. The resulting enormous reproductive output may contribute to explain why some genera of social insects became so successful. Indeed, superorganismal ant lineages have more species than those that have not passed a MET. We conclude that the release from life history constraints at the individual level is a important, yet understudied, factor across METs to explain their evolutionary success.

Genome-Wide SNP Analysis of Male and Female Rice Field Frogs, Hoplobatrachus rugulosus, Supports a Non-Genetic Sex Determination System

Sex determination systems (SDSs) in anurans are diverse and have undergone independent evolutionary transitions among species. The mode of sexual reproduction of the rice field frog (Hoplobatrachus rugulosus)—an economically viable, edible amphibian species—is not well known. Previous studies have proposed that threshold temperature conditions may determine sex in these frogs. To elucidate the SDS in H. rugulosus, we karyotyped 10 male and 12 female frogs, and performed fluorescence in situ hybridization combined with sequencing analyses using DArTseq™. Our results revealed a highly conserved karyotype with no sex chromosome heteromorphism, and the sequencing analyses did not identify any consistent sex-linked loci, supporting the hypothesis of temperature-dependent sex determination. The results of this study, and others, on SDSs in the rice field frog and related species also provide support for the theory that heteromorphic sex chromosomes may lead to an evolutionary trap that prevents variable SDSs. These findings add important information to the body of knowledge on H. rugulosus and are likely to have a significant impact on the productivity and economic success of rice field frog farming.

Evolution of flower color genes in petunias and their wild relatives

Evolutionary transitions in flower color often trace back to changes in the flavonoid biosynthetic pathway and its regulators. In angiosperms, this pathway produces a range of red, purple, and blue anthocyanin pigments. Transcription factor (TF) complexes involving members of the MYB, bHLH, and WD40 protein families control the expression of pathway enzymes. Here, we investigate flavonoid pathway evolution in the Petunieae clade of the tomato family (Solanaceae). Using transcriptomic data from 69 species of Petunieae, we estimated a new phylogeny for the clade. For the 65 species with floral transcriptomes, we retrieved transcripts encoding homologs of 18 enzymes and transcription factors to investigate patterns of evolution across genes and lineages. We found that TFs exhibit faster rates of molecular evolution than their targets, with the highly specialized MYB genes evolving fastest. Using the largest comparative dataset to date, we recovered little support for the hypothesis that upstream enzymes evolve slower than those occupying more downstream positions. However, expression levels inversely correlated with molecular evolutionary rates, while shifts in floral pigmentation were weakly related to changes affecting coding regions. Nevertheless, shifts in floral pigmentation and presence/absence patterns of MYB transcripts are strongly correlated. Intensely pigmented and patterned species express homologs of all three main MYB anthocyanin activators in petals, while pale or white species express few or none. Our findings reinforce the notion that regulators of the flavonoid pathway have a dynamic history, involving higher rates of molecular evolution than structural components, along with frequent changes in expression during color transitions.

Extremely reduced supergroup F Wolbachia: transition to obligate insect symbionts

Wolbachia are widely distributed symbionts among invertebrates that manifest by a broad spectrum of lifestyles from parasitism to mutualism. Wolbachia Supergroup F is considered a particularly interesting group which gave rise to symbionts of both arthropods and nematodes, and some of its members are obligate mutualists. Further investigations on evolutionary transitions in symbiosis have been hampered by a lack of genomic data for Supergroup F members. In this study, we present genomic data for five new supergroup F Wolbachia strains associated with four chewing lice species. These new strains in different evolutionary stages show genomic characteristics well-illustrating the evolutionary trajectory which symbiotic bacteria experience during their transition to mutualism. Three of the strains have not yet progressed with the transition, the other two show typical signs of ongoing gene deactivation and removal (genome size, coding density, low number of pseudogenes). Particularly, wMeur1, a symbiont fixed in all Menacanthus eurystenus populations across four continents, possesses a highly reduced genome of 733,850 bp with a horizontally acquired capacity for pantothenate synthesis. Comparing with other strains showed wMeur1 genome as the smallest currently known among all Wolbachia and the first example of Wolbachia which has completed genomic streamlining known from the gammaproteobacterial obligate symbionts.