How Do Genomes Create Novel Phenotypes? Insights from the Loss of the Worker Caste in Ant Social Parasites

Abstract

A central goal of biology is to uncover the genetic basis for the origin of new phenotypes. A particularly effective approach is to examine the genomic architecture of species that have secondarily lost a phenotype with respect to their close relatives. In the eusocial Hymenoptera, queens and workers have divergent phenotypes that may be produced via either expression of alternative sets of caste-specific genes and pathways or differences in expression patterns of a shared set of multifunctional genes. To distinguish between these two hypotheses, we investigated how secondary loss of the worker phenotype in workerless ant social parasites impacted genome evolution across two independent origins of social parasitism in the ant genera Pogonomyrmex and Vollenhovia. We sequenced the genomes of three social parasites and their most-closely related eusocial host species and compared gene losses in social parasites with gene expression differences between host queens and workers. Virtually all annotated genes were expressed to some degree in both castes of the host, with most shifting in queen-worker bias across developmental stages. As a result, despite >1 My of divergence from the last common ancestor that had workers, the social parasites showed strikingly little evidence of gene loss, damaging mutations, or shifts in selection regime resulting from loss of the worker caste. This suggests that regulatory changes within a multifunctional genome, rather than sequence differences, have played a predominant role in the evolution of social parasitism, and perhaps also in the many gains and losses of phenotypes in the social insects.

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

“…The sequencing of more species with different levels of plasticity and multiple phenotypes will be required to confirm this hypothesis (6). However, the available data suggest that these hallmarks contrast with those hallmarks of eusocial insects with low plasticity like the honey bee and most ants, where a large proportion of genes, functionality, and network differentiation are associated with phenotypic differentiation (44,(53)(54)(55)(56)(57)(58), and where phenotypes appear to be regulated by DNA methylation (24,25,30,34,35,37,(59)(60)(61)(62). Comparisons of species with contrasting evolutionary histories, as in our study species, will be especially valuable in revealing the molecular signatures at the origin of social evolution (e.g., in P. canadensis) and in reversions from complex to simple behaviors (e.g., in D. quadriceps).…”

Convergent evolution of the army ant syndrome and congruence in big-data phylogenetics

“…In addition to sampling all doryline genera, species from all biogeographic regions (as defined in (Cox, 2001) but treating the Malagasy region separate from Afrotropical) were included for each major lineage. Nine outgroup and one ingroup species (Ooceraea biroi) were also included based on publicly available ant genomes: Atta cephalotes (Suen et al, 2011), Camponotus foridanus (Bonasio et al, 2010), Cardiocondyla obscurior (Schrader et al, 2014), Harpegnathos saltator (Bonasio et al, 2010), Linepithema humile (Smith et al, 2011a), Ooceraea biroi (Oxley et al, 2014), Pogonomyrmex barbatus (Smith et al, 2011b), Solenopsis invicta (Wurm et al, 2011), and Vollenhovia emeryi (Smith et al, 2015).…”

Limited social plasticity in the socially polymorphic sweat bee Lasioglossum calceatum

“…Phenotypic plasticity can be lost via genetic drift and subsequent genetic assimilation once environmental conditions become predictable (Masel et al 2007; Pfennig et al 2010), and when circumstances in which the alternative phenotype is expressed no longer arise (Sikkink et al 2014; Smith et al 2015; Cini et al 2015). At Inverness, B1 females always enter hibernation, whereas at Sussex they may either become workers or enter hibernation (Davison and Field 2016).…”

“…It is thought that such reversals could be driven by selection acting on only a small number of regulatory switches (West-Eberhard 2003), and that in transitional populations initial plasticity in social phenotype might be lost once environmental conditions become predictable (Field et al 2010; Cini et al 2015; Smith et al 2015). Therefore, a key question is to what extent alternative eusocial and solitary phenotypes result from environmentally mediated plasticity or represent distinct, genetically fixed alternatives (Wcislo 1997).…”