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. 2008 Nov 18;105(46):17884-9.
doi: 10.1073/pnas.0807351105. Epub 2008 Nov 12.

Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies

Abderrahman Khila  1 , Ehab Abouheif
Affiliations

Reproductive constraint is a developmental mechanism that maintains social harmony in advanced ant societies

Abderrahman Khila et al. Proc Natl Acad Sci U S A. .

Abstract

A hallmark of eusociality in ants is the reproductive division of labor between queens and workers. Yet, nothing is known about the molecular mechanisms underlying reproduction in this group. We therefore compared the developmental genetic capacity of queens and workers to reproduce in several eusocially advanced species from the two largest subfamilies of ants, the Myrmicinae and Formicinae. In flies, the asymmetric localization of maternally encoded determinants (mRNAs and proteins) during oogenesis establishes oocyte polarity and subsequently ensures proper embryonic development. Vasa and nanos, two key maternal determinants, are properly localized in the posterior of queen oocytes, but their localization is impaired in those of the workers. This mislocalization leads to severe embryonic defects in worker progeny, and therefore, represents a constraint on worker reproduction that we call 'reproductive constraint.' We show that reproductive constraint is phylogenetically widespread, and is at high levels in most species tested. Reproductive constraint can simultaneously reduce or eliminate the workers' ability to produce viable eggs for reproduction, while preserving their ability to produce trophic eggs for nutrition, and thus, may have been the basis for the evolutionary retention of worker ovaries in the majority of ants. We propose that high levels of reproductive constraint has most likely evolved as a consequence of selection at the colony level to reduce or eliminate any potential conflict over worker reproduction, therefore maintaining harmony and colony efficiency in advanced ant societies.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Cellular and molecular organization of queen and worker ovarioles in ants. Green color marks Vasa expression, red marks F-actin, and blue marks nuclei. (A) simplified schematic diagram showing the organization of the germ line in ant queen ovarioles. Germ-line stem cells (GSCs), located at the anterior tip of each adult ovariole, divide to give rise to cystoblasts (Cb), which in turn undergo five incomplete divisions to become 32-cell cysts. One cell acquires the oocyte fate whereas the remaining 31 cells become polyploid nurse cells. The cells forming each cyst are interconnected by fusomes; cytoskeletal bridges through which maternal determinants are transported from the nurse cells to the oocyte. Maternal determinants, including mRNAs and proteins, establish oocyte polarity and set up embryonic development. (B) A. rudis queen ovariole showing the anterior half from the terminal filament (TF) to early egg chambers. Dashed lines indicate the continuation of the ovariole. (C) A. rudis worker ovariole showing identical cellular and molecular organization to the queen. BI, BII, BIII, and CI, CII, CIII represent zooms of the regions indicated by B1, B2, B3, and C1, C2, C3, respectively. Both queens and workers show normal cystoblast production (B1 and C1), normal and continuous cyst production (B2 and C2), and proper establishment of oocyte identity and egg chamber formation (B3 and C3). Note that the ovariole of the queen (B) is longer than that of the worker (C), because of its higher activity. Cells from germ-line origin in both queens and workers, including GSC and their progeny, as well as the nurse cells express Vasa, whereas cells from somatic origin including TF, cap (CC), and follicle cells (FC) do not.
Fig. 2.
Fig. 2.
Patterns of Vasa and nanos expression and localization in queen and worker oocytes. Green color marks Vasa protein; red marks F-actin in A–G, and nanos mRNA in K–M; purple marks nanos mRNA in B and H–J; and blue marks nuclei. Arrow heads indicate correct localization, asterisks indicate impaired localization; NC nurse cells; Oo, oocyte. In queens, posterior localization of (A) Vasa and (B) nanos (red) indicate viable oocytes, whereas the lack of (C) Vasa localization indicate trophic oocytes. In workers, proper localization to the posterior of (D) Vasa and (H) nanos (purple) indicate viable oocytes; mis-localized (F) Vasa and (I) nanos (purple) indicate failed oocytes; and absence of (G) Vasa and (J) nanos (purple) indicate trophic oocytes. (K–M) double Vasa and nanos (red) in worker oocytes. (K) nanos is localized early in worker oocytes, followed later by the posterior (I) Vasa localization. (M) Both molecules remain colocalized while detaching from the posterior in late stages. Note that the yellow color in the follicle cells in E and G results from high background from the green channel, rather than Vasa expression in these cells.
Fig. 3.
Fig. 3.
Molecular and morphological assessment of embryonic development in M. americana queen- and worker-laid eggs. Green marks Vasa protein; blue marks nuclei; arrow heads indicate normal structures, whereas asterisks indicate morphological or molecular defects. (A, E, and I) Embryos produced by the queen, shown at different developmental stages, undergo normal development. (B) Vasa protein, which is inherited from the mother during oogenesis, is properly localized in early embryos and is normally expressed in the germ line throughout development (F and J). Embryos produced by the workers show (C) disorganized cytoskeleton, as well as (G and K) severe axis defects during various stages of embryogenesis. (D) Worker embryos have inherited Vasa localization defects from their mothers, and fail to initiate or complete (H and L) subsequent embryogenesis stages.
Fig. 4.
Fig. 4.
The evolutionary dynamic of reproductive constraint in ants. Phylogenetic relationships were based on ref. . The asterisks indicate the three focal species. The unconstrained reproduction of solitary insects and ant queens is represented by a green oocyte diagram showing proper localization of maternal determinants. The constrained reproduction in the workers of several ant species within the formicines and myrmicines is represented by a red oocyte diagram showing impaired maternal determinant localization. The oocyte diagram at particular nodes represents the likely state of the ancestor of formicines and myrmicines, and of hymenopterans. The length of the red bars reflects the level and percentage of constraint, which was calculated as the number of failed oocytes divided by the total number of failed and viable oocytes produced by orphaned workers. Trophic oocytes were excluded.
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