Embryogenesis in myrmicine ants combines features of short and long germ-band modes of development

Abstract

Ants exhibit complex social organization, morphologically distinct castes with division of labor, and the exploitation of diverse ecological niches. The extent to which these features have influenced embryonic development relative to other insects remains unclear. Insect embryogenesis has been classified into one of three modes: long, short, and intermediate germ-band. In long germ-band development, exemplified by the fruit fly Drosophila melanogaster, segments along the entire anterior-posterior axis of the embryonic primordium are established almost simultaneously, prior to gastrulation, with the initial embryonic primordium surrounding almost the entire volume of the egg. In short and intermediate germ-band modes, the embryonic primordium occupies a smaller proportion of the egg surface, with anterior segments initially specified, and remaining segments being added sequentially from a posterior growth zone. Here, we show a novel pattern of development in three myrmicine ants, the fungus-gardening ants Atta texana and Mycocepurus smithii, and the red imported fire ant Solenopsis invicta. Early in embryogenesis, they exhibit features of short germ-band development, while later in development they exhibit a newly-characterized progressive pattern of segmentation that has been associated with some long germ-band-developing insects. Moreover, despite similarities in the size of ant and Drosophila eggs, the duration of embryogenesis in the three ant species is 10 to 20-fold longer than in Drosophila and is also significantly longer than in the honeybee Apis mellifera and the jewel wasp Nasonia vitripennis. In addition, the embryos produced by A. texana foundress queens develop to first instar larvae 25% faster than embryos produced by mature queens. We discuss these results in the context of the eusocial lifestyle of ants.