The build-up of dominance hierarchies in eusocial insects

Reproductive division of labour is a hallmark of eusocial insects. However, its stability can often be hampered by the potential for reproduction by otherwise sterile nest-mates. Dominance hierarchy has a crucial role in some species in regulating which individuals reproduce. Compared with those in vertebrates, the dominance hierarchies in eusocial insects tend to involve many more individuals, and should require additional selective forces unique to them. Here, we provide an overview of a series of studies on dominance hierarchies in eusocial insects. Although reported from diverse eusocial taxa, dominance hierarchies have been extensively studied in paper wasps and ponerine ants. Starting from molecular physiological attributes of individuals, we describe how the emergence of dominance hierarchies can be understood as a kind of self-organizing process through individual memory and local behavioural interactions. The resulting global structures can be captured by using network analyses. Lastly, we argue the adaptive significance of dominance hierarchies from the standpoint of sterile subordinates. Kin selection, underpinned by relatedness between nest-mates, is key to the subordinates' acceptance of their positions in the hierarchies. This article is part of the theme issue ‘The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies’.

Fertility Outcomes, Heritability and Genomic Associations of In-Group Preference and In-Group Marriage

Using data from the Midlife Development in the USA (MIDUS) sample (3070 men and 3182 women) and the Wisconsin Longitudinal Study (WLS; 2240 men and 2346 women), we aimed to investigate whether religious, ethnic and racial in-group preferences as well as religious homogamy are associated with reproductive outcome in terms of number of children. Using data from the MIDUS twin sample, we further estimated the inherited genetic component of in-group attitudes. Additionally, we analyzed the association of ∼50 polygenic scores (PGSs) recently published for the WLS study and in-group attitudes as an indicator of potential pleiotropic effects. We found in both samples that, with one exception, religious though not other in-group attitudes are associated with a higher reproductive outcome. Also, religious homogamy is associated with higher average number of children. The inherited component of all in-group attitudes ranges from ∼21% to 45% (MIDUS twin sample). PGSs associated with religious behavior are significantly positively associated with religious in-group attitudes as well as family attitudes. Further associations are found with PGS on life satisfaction (work) and, negatively, with PGS for any sort of addiction (smoking, alcohol and cannabis use), indicating pleiotropy. We conclude that the positive association between religious in-group attitudes as well as religious homogamy and reproductive outcome may indicate selective forces on religious in-group behavior. As all investigated in-group attitudes, however, have a substantial inherited component, we further speculate that potential previous reproductive benefits of racial and ethnic in-group preferences, if they ever existed, might have been substituted by religious in-group preferences.

A PRELIMINARY COMPARISON OF MITOCHONDRIAL D-LOOP REGION OF FUNAAB ALPHA AND NIGERIAN INDIGENOUS CHICKENS

Nigerian indigenous chickens possess immunity from endemic diseases and have a better survival rate than commercial hybrid strains under local production conditions. FUNAAB Alpha chicken was developed by improving Nigerian indigenous chickens through crossbreeding and selection. This study compared the mitochondrial d-loop of FUNAAB Alpha and Nigerian indigenous chickens to check likely genetic erosion and loss of diversity in development of FUNAAB Alpha breed. Blood samples were collected from Nigerian indigenous (n=23) and FUNAAB Alpha (n=20) chickens sampled from farms and houses in Ogun state, Nigeria. The Hypervariable 1 (HV1) of the mitochondrial d-loop region was amplified and sequenced. Single nucleotide polymorphisms present in HV1 of chickens were identified using Clustal W. Genetic diversity of the region was determined using DnaSp v5 while selective forces acting on the chickens were predicted using HyPhy software implemented inside MEGA 6 software. Phylogenetic relationship among FUNAAB Alpha, Nigerian indigenous and other chicken breeds was determined using MEGA 6 software. Five polymorphisms were identified in FUNAAB Alpha chickens while twelve were identified in Nigerian indigenous chickens. All the polymorphisms identified in FUNAAB Alpha chickens were also observed in Nigerian indigenous chickens while seven polymorphisms were unique to Nigerian indigenous chickens. Higher diversity indices were observed in Nigerian indigenous chickens (number of haplotype: 4; haplotype diversity: 0.743±0.012; nucleotide diversity: 0.014±0.0013 and average number of nucleotide differences: 4.332) compared with FUNAAB Alpha chickens (number of haplotype: 2; haplotype diversity: 0.485±0.001; nucleotide diversity: 0.008±0.0001 and average number of nucleotide differences: 2.424). Positive selective forces were acting on FUNAAB Alpha chickens while negative selective forces were acting on Nigerian indigenous chickens. Phylogenetic analysis revealed that FUNAAB Alpha chickens clustered with Nigerian indigenous and South American chickens. It can be concluded that there was likely genetic erosion and loss of diversity in development of FUNAAB Alpha breed. Breeding programmes aimed at improvement of genetic diversity and reduction of genetic erosion should be applied in subsequent improvement of FUNAAB Alpha chickens.

Evolution of Natural Lifespan Variation and Molecular Strategies of Extended Lifespan

To understand the genetic basis and the selective forces acting on longevity, it is useful to employ ecologically diverse individuals of the same species, widely different in lifespan. This way, we may capture the experiment of Nature that modifies the genotype arriving at different lifespans. Here, we analyzed 76 ecologically diverse wild yeast isolates and discovered wide diversity of lifespan. We sequenced the genomes of these organisms and analyzed how their replicative lifespan is shaped by nutrients and transcriptional and metabolite patterns. By identifying genes, proteins and metabolites that correlate with longevity across these isolates, we found that long-lived strains elevate intermediary metabolites, differentially regulate genes involved in NAD metabolism and adjust control of epigenetic landscape through conserved, rare histone modifier. Our data further offer insights into the evolution and mechanisms by which caloric restriction regulates lifespan by modulating the availability of nutrients without decreasing fitness.

Homo Paedens? Did Kids Invent the Human Species?

The evolution of development (“evo-devo”) has become a central concern in both evolu­tionary and developmental research, and human immaturity is no less a proper focus for evolutionary analysis than that of other species-if anything, it is more so. Two new books by David F. Bjorklund, a founder of evolutionary developmental psychology, summarize what we know now and propose that children invented our species. Due to the new phe­nomenon of partly heritable epigenetic modification of genes and the old one of the Bald­win Effect (by which plasticity leads to new selective forces on genes), this claim must be at least partly true. The inherent plasticity of children’s behavior, including play, accelerat­ed the evolution of humanity as instantiated in the human brain. Evolution cannot be understood without extensive reference to development, and nothing in childhood makes sense except in the light of evolution.

Medawar and Hamilton on the selective forces in the evolution of ageing

Both Medawar and Hamilton contributed key ideas to the modern evolutionary theory of ageing. In particular, they both suggested that, in populations with overlapping generations, the force with which selection acts on traits declines with the age at which traits are expressed. This decline would eventually cause ageing to evolve. However, the biological literature diverges on the relationship between Medawar’s analysis of the force of selection and Hamilton’s. Some authors appear to believe that Hamilton perfected Medawar’s insightful, yet ultimately erroneous analysis of this force, while others see Hamilton’s analysis as a coherent development of, or the obvious complement to Medawar’s. Here, the relationship between the two analyses is revisited. Two things are argued for. First, most of Medawar’s alleged errors that Hamilton would had rectified seem not to be there. The origin of these perceived errors appears to be in a misinterpretation of Medawar’s writings. Second, the mathematics of Medawar and that of Hamilton show a significant overlap. However, different meanings are attached to the same mathematical expression. Medawar put forth an expression for the selective force on age-specific fitness. Hamilton proposed a full spectrum of selective forces each operating on age-specific fitness components, i.e. mortality and fertility. One of Hamilton’s expressions, possibly his most important, is of the same form as Medawar’s expression. But Hamilton’s selective forces on age-specific fitness components do not add up to yield Medawar’s selective force on age-specific fitness. It is concluded that Hamilton’s analysis should be considered neither as a correction to Medawar’s analysis nor as its obvious complement.

Evolution of natural lifespan variation and molecular strategies of extended lifespan

To understand the genetic basis and selective forces acting on longevity, it is useful to examine lifespan variation among closely related species, or ecologically diverse isolates of the same species, within a controlled environment. In particular, this approach may lead to understanding mechanisms underlying natural variation in lifespan. Here, we analyzed 76 ecologically diverse wild yeast isolates and discovered a wide diversity of replicative lifespan. Phylogenetic analyses pointed to genes and environmental factors that strongly interact to modulate the observed aging patterns. We then identified genetic networks causally associated with natural variation in replicative lifespan across wild yeast isolates, as well as genes, metabolites and pathways, many of which have never been associated with yeast lifespan in laboratory settings. In addition, a combined analysis of lifespan-associated metabolic and transcriptomic changes revealed unique adaptations to interconnected amino acid biosynthesis, glutamate metabolism and mitochondrial function in long-lived strains. Overall, our multi-omic and lifespan analyses across diverse isolates of the same species shows how gene-environment interactions shape cellular processes involved in phenotypic variation such as lifespan.

The molecular evolution of spermatogenesis across mammals

The testis is a key male reproductive organ that produces gametes through the process of spermatogenesis. Testis morphologies and spermatogenesis evolve rapidly in mammals, presumably due to the evolutionary pressure on males to be reproductively successful. The rapid evolution of the testis was shown to be reflected at the molecular level based on bulk-tissue work, but the molecular evolution of individual spermatogenic cell types across mammalian lineages remains largely uncharacterized. Here we report evolutionary analyses of single-nucleus transcriptome data for testes from eleven species that cover the three major mammalian lineages (eutherians, marsupials, egg-laying monotremes) and birds (the evolutionary outgroup), and include seven key primates. Our analyses reveal that the rapid evolution of the testis is driven by accelerated fixation rates of gene expression changes, amino acid altering substitutions, and newly emerged genes in late spermatogenic stages - likely facilitated by reduced pleiotropic constraints, haploid selection, and a transcriptionally permissive chromatin environment. We identify temporal expression changes of individual genes across species, which may have contributed to the emergence of species-specific phenotypes, but also conserved expression programs underlying ancestral spermatogenic processes. Sex chromosome analyses show that genes predominantly expressed in spermatogonia (i.e., germ cells fueling spermatogenesis) and Sertoli cells (i.e., somatic supporting cells) independently accumulated on X chromosomes across mammals during evolution, presumably due to male-beneficial selective forces. Further work uncovered that the process of meiotic sex chromosome inactivation (MSCI) also occurs in monotremes and hence is common to the different mammalian sex chromosome systems, contrary to previous inferences. Thus, the general mechanism of meiotic silencing of unsynapsed chromatin (MSUC), which underlies MSCI, represents an ancestral mammalian feature. Together, our study illuminates the cellular and molecular evolution of mammalian spermatogenesis and associated selective forces, and provides a resource for investigating the biology of the testis across mammals.

Repeats Mimic Immunostimulatory Viral Features Across a Vast Evolutionary Landscape

An emerging hallmark across many human diseases – such as cancer, autoimmune and neurodegenerative disorders – is the aberrant transcription of typically silenced repetitive elements. Once transcribed they can mimic pathogen-associated molecular patterns and bind pattern recognition receptors, thereby engaging the innate immune system and triggering inflammation in a process known as viral mimicry. Yet how to quantify pathogen mimicry, and the degree to which it is shaped by natural selection, remains a gap in our understanding of both genome evolution and the immunological basis of disease. Here we propose a theoretical framework that combines recent biological observations with statistical physics and population genetics to quantify the selective forces on virus-like features generated by repeats and integrate these forces into predictive evolutionary models. We establish that many repeat families have evolutionarily maintained specific classes of viral mimicry. We show that for HSATII and intact LINE-1 selective forces maintain CpG motifs, while for a set of SINE and LINE elements the formation of long double-stranded RNA is more prevalent than expected from a neutral evolutionary model. We validate our models by showing predicted immunostimulatory inverted SINE elements bind the MDA5 receptor under conditions of epigenetic dysregulation and that they are disproportionately present during intron retention when RNA splicing is pharmacologically inhibited. We conclude viral mimicry is a general evolutionary mechanism whereby genomes co-opt features generated by repetitive sequences to trigger the immune system, acting as a quality control system to flag genome dysregulation. We demonstrate these evolutionary principles can be learned and applied to predictive models. Our work therefore serves as a resource to identify repeats with candidate immunostimulatory features and leverage them therapeutically.

When and Why Did Human Brains Decrease in Size? A New Change-Point Analysis and Insights From Brain Evolution in Ants

Human brain size nearly quadrupled in the six million years since Homo last shared a common ancestor with chimpanzees, but human brains are thought to have decreased in volume since the end of the last Ice Age. The timing and reason for this decrease is enigmatic. Here we use change-point analysis to estimate the timing of changes in the rate of hominin brain evolution. We find that hominin brains experienced positive rate changes at 2.1 and 1.5 million years ago, coincident with the early evolution of Homo and technological innovations evident in the archeological record. But we also find that human brain size reduction was surprisingly recent, occurring in the last 3,000 years. Our dating does not support hypotheses concerning brain size reduction as a by-product of body size reduction, a result of a shift to an agricultural diet, or a consequence of self-domestication. We suggest our analysis supports the hypothesis that the recent decrease in brain size may instead result from the externalization of knowledge and advantages of group-level decision-making due in part to the advent of social systems of distributed cognition and the storage and sharing of information. Humans live in social groups in which multiple brains contribute to the emergence of collective intelligence. Although difficult to study in the deep history of Homo, the impacts of group size, social organization, collective intelligence and other potential selective forces on brain evolution can be elucidated using ants as models. The remarkable ecological diversity of ants and their species richness encompasses forms convergent in aspects of human sociality, including large group size, agrarian life histories, division of labor, and collective cognition. Ants provide a wide range of social systems to generate and test hypotheses concerning brain size enlargement or reduction and aid in interpreting patterns of brain evolution identified in humans. Although humans and ants represent very different routes in social and cognitive evolution, the insights ants offer can broadly inform us of the selective forces that influence brain size.