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.
Highlights
Division of labor is the cornerstone of insect societies and implies the coexistence of individuals that differ in morphology, reproduction and behavior [1,2]
The two Vg genes have an identical number of exons (Figure 1A) and share the three structural domains typical of vitellogenins: the lipoprotein N-terminal domain (LPD-N), the domain of unknown function 143 (DUF1943) and the von Willebrand factor type D domain (VWD) [35,36] (Figure 1B)
To determine whether the presence of multiple Vg genes is a general feature of ants, we searched for Vg genes in the five additional recently published ant genomes
Summary
Division of labor is the cornerstone of insect societies and implies the coexistence of individuals that differ in morphology, reproduction and behavior [1,2]. There are usually two levels of division of labor among individuals in social insect colonies. The first relates to a reproductive division of labor, whereby reproduction is monopolized by one or several queens while sterile workers perform all the tasks related to colony maintenance. The second relates to a division of labor among the worker force, whereby workers perform different tasks in an age-dependent sequence: young workers usually perform tasks inside the colony (e.g. brood care) while old workers forage outside the nest [3,4]. While the ecological constraints favoring social evolution are well studied [7], it remains largely unknown whether the genetic mechanisms regulating behavior are conserved among species [8,9,10,11,12]
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