Vitellogenin Underwent Subfunctionalization to Acquire Caste and Behavioral Specific Expression in the Harvester Ant Pogonomyrmex barbatus

Abstract

The reproductive ground plan hypothesis (RGPH) proposes that the physiological pathways regulating reproduction were co-opted to regulate worker division of labor. Support for this hypothesis in honeybees is provided by studies demonstrating that the reproductive potential of workers, assessed by the levels of vitellogenin (Vg), is linked to task performance. Interestingly, contrary to honeybees that have a single Vg ortholog and potentially fertile nurses, the genome of the harvester ant Pogonomyrmex barbatus harbors two Vg genes (Pb_Vg1 and Pb_Vg2) and nurses produce infertile trophic eggs. P. barbatus, thus, provides a unique model to investigate whether Vg duplication in ants was followed by subfunctionalization to acquire reproductive and non-reproductive functions and whether Vg reproductive function was co-opted to regulate behavior in sterile workers. To investigate these questions, we compared the expression patterns of P. barbatus Vg genes and analyzed the phylogenetic relationships and molecular evolution of Vg genes in ants. qRT-PCRs revealed that Pb_Vg1 is more highly expressed in queens compared to workers and in nurses compared to foragers. By contrast, the level of expression of Pb_Vg2 was higher in foragers than in nurses and queens. Phylogenetic analyses show that a first duplication of the ancestral Vg gene occurred after the divergence between the poneroid and formicoid clades and subsequent duplications occurred in the lineages leading to Solenopsis invicta, Linepithema humile and Acromyrmex echinatior. The initial duplication resulted in two Vg gene subfamilies preferentially expressed in queens and nurses (subfamily A) or in foraging workers (subfamily B). Finally, molecular evolution analyses show that the subfamily A experienced positive selection, while the subfamily B showed overall relaxation of purifying selection. Our results suggest that in P. barbatus the Vg gene underwent subfunctionalization after duplication to acquire caste- and behavior- specific expression associated with reproductive and non-reproductive functions, supporting the validity of the RGPH in ants.

Molecular traces of alternative social organization in a termite genome

“…5), suggesting it has a function outside oogenesis. This is similar to the expanded functionality observed in duplicated Vgs in the ants Solenopsis invicta and P. barbatus 9,39 . In these cases, as with the honey bee, Vg appears to have acquired a role in regulating behavioural caste, and a similar function may have developed in Z. nevadensis.…”

Eusocial insects as emerging models for behavioural epigenetics

“…Unlike honeybees and ponerine ants (for example, H. saltator), the genomes of which have one vg gene locus, multiple vg paralogues have been identified in myrmicine ants (for example, Pogonomyrmex barbatus) and dolichoderine ants (for example, Linepithema humile). Expression analyses of these paralogues suggest that functional divergence of Vg is linked to behavioural specializations specifically in more advanced ant species 157 .…”

Why do social insect queens live so long? Approaches to unravel the sociality-aging puzzle

“…However, some components of these pathways (such as vitellogenin) might have acquired additional functions [28][29][30][31][32]. Making use of all available genomic resources and technological advances, an integrative, standardized experimental approach will help gain a comprehensive understanding of the molecular basis underlying the reshaping of the fecundity/longevity trade-off in social insects.…”