bioRxiv Science⌕ Search

bioRxiv · 10.1101/604470

Macroevolutionary integration of phenotypes within and across ant worker castes

Abstract

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intra- and inter-caste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.

Source connections

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Friedman, N. R., Bennet, B. L., Fischer, G., Sarnat, E. M., Huang, J.-P., Knowles, L. L., Economo, E. P.. 2019-04-11. Macroevolutionary integration of phenotypes within and across ant worker castes. https://doi.org/10.1101/604470

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

A timeline for evolution of metabolism in early microbes

The metabolism of early microbes shaped our planet's chemistry and enabled more life to evolve. However, it remains uncertain when many forms of metabolism arose and which organisms carried them out. Here we combine machine learning, metabolic networks, and phylogenomics of microbes to date 14 forms of metabolism and 6 other traits. We find that metabolism evolved in three waves, starting >3.4 billion years ago (Ga) with fermentation and sulfur compound respiration. A second wave began ~3.2 Ga with aerobic respiration and growth, while a third began ~1.4 Ga with further specialization. We compared these predictions with independent dates from the geochemical record, and agreement with conservative dates was good (CCC = 0.81 to 0.89). Several forms of metabolism are invisible in the geochemical record, and our approach dates these forms, too. Our results reconcile different lines of evidence for microbial evolution and provide a fuller picture of early Earth.

evolutionary biology↗

Sexual interactions and local selection shape reproductive gene diversity and divergence

Genes involved in genotype x genotype coevolution display unique patterns of nucleotide diversity and population divergence. In Drosophila melanogaster, Sex Peptide is a key sperm competition gene that is an outlier for both pi within populations and Fst between populations. This pattern is not predicted by current theoretical expectations of selective sweeps highlighting the need to develop predictions to identify genes experiencing balancing selection. We compared pi and FST in D. melanogaster populations to identify other genes following a co-evolutionary model that generates divergence and diversity. Multiple male and female genes that interact with Sex Peptide exhibited elevated FST x pi values. Genome-wide analyses also revealed an enrichment of genes critical for neuronal development, pointing to courtship evolution. Specifically, fruitless, its interacting genes, and a female behavior gene were identified as outliers. These parallel findings indicate that both sperm competition and mating behaviors are subject to co-evolutionary selection.

evolutionary biology↗

How Fisherian runaway halts: Genomic architecture determines the long-term evolutionary consequences of sexual selection.

Sexual selection explains the evolution of exaggerated sexual displays, but less obvious is why biased mate preferences--a requirement for sexual selection--evolve. Fisher (1930) proposed that biased mate preferences can spark self-reinforcing evolutionary process (runaway) that drives their own evolution. This occurs because mate choice imposes sexual selection on sexual displays and links them genetically to mate preferences, producing indirect selection on the preferences themselves. While mathematical models have demonstrated the plausibility of the runaway theory, they rely on several idealized assumptions. Consequently, it remains poorly understood how runaway halts once populations deviate from these idealized conditions as a consequence of evolution via runaway, and how the genetic architecture underlying sexual displays influences the resulting evolutionary dynamics. Here, we address these gaps using two complementary approaches. First, we review and synthesize existing theories to classify the mechanisms that halt runaway into four categories, based on which idealized assumptions of Lande's (1981) classic model are violated during evolution via runaway. Second, we conduct individual-based evolutionary simulations varying the genetic architecture of sexual displays from conventional additive to omnigenic inheritance models. Our results show that genetic architecture determines how runaway process halts, thereby governing long-term evolutionary dynamics under sexual selection.

evolutionary biology↗