Department of Biology, McGill University, Montreal, Quebec, Canada.
Whitehead Institute for Biomedical Research, Cambridge, Massachusetts, USA.
J Exp Zool B Mol Dev Evol. 2024 Dec;342(8):557-585. doi: 10.1002/jez.b.23278.
Ants are one of the most ecologically and evolutionarily successful groups of animals and exhibit a remarkable degree of phenotypic diversity. This success is largely attributed to the fact that all ants are eusocial and live in colonies with a reproductive division of labor between morphologically distinct queen and worker castes. Yet, despite over a century of studies on caste determination and evolution in ants, we lack a complete ontogenetic series from egg to adult for any ant species. We, therefore, present a developmental table for the Pharaoh ant Monomorium pharaonis, a species whose colonies simultaneously produce reproductive queens and completely sterile workers. In total, M. pharaonis embryonic, larval, and pupal development lasts 45 days. During embryogenesis, the majority of developmental events are conserved between M. pharaonis and the fruit fly Drosophila melanogaster. We discovered, however, two types of same-stage embryos before gastrulation: (1) embryos with internalized germ cells; and (2) embryos with germ cells outside of the blastoderm at the posterior pole. Moreover, we also found two-types of embryos following germ band extension: (1) embryos with primordial germ cells that will develop into reproductive queens; and (2) embryos with no germ cells that will develop into completely sterile workers. Together, these data show that queen and worker castes are already determined and differentiated by early embryogenesis. During larval development, we confirmed that reproductive and worker larvae proceed through three larval instars. Using anatomical and developmental markers, we can further discern the development of gyne (unmated queen) larvae, male larvae, and worker larvae as early as the 1st instar. Overall, we hope that the ontogenetic series we present here will serve as a blueprint for the generation of future ant developmental tables.
蚂蚁是动物界中生态和进化最成功的群体之一,表现出显著的表型多样性。这种成功在很大程度上归因于所有蚂蚁都是真社会性的,生活在具有生殖分工的蚁群中,形态上有明显区别的蚁后和工蚁。然而,尽管对蚂蚁的等级决定和进化进行了一个多世纪的研究,但我们缺乏任何蚂蚁物种从卵到成虫的完整个体发生系列。因此,我们展示了法老蚁 Monomorium pharaonis 的发育表,该物种的蚁群同时产生有生殖能力的蚁后和完全不育的工蚁。总的来说,M. pharaonis 的胚胎、幼虫和蛹期发育持续 45 天。在胚胎发生过程中,大多数发育事件在 M. pharaonis 和果蝇 Drosophila melanogaster 之间是保守的。然而,我们在原肠胚形成之前发现了两种同阶段的胚胎:(1)内部化的生殖细胞的胚胎;和(2)位于胚盘后端的外部生殖细胞的胚胎。此外,我们还发现了两种类型的原肠胚延伸后胚胎:(1)具有将发育成生殖蚁后的原始生殖细胞的胚胎;和(2)没有生殖细胞的胚胎,将发育成完全不育的工蚁。这些数据表明,蚁后和工蚁等级在早期胚胎发生时就已经确定和分化。在幼虫发育过程中,我们证实生殖蚁和工蚁幼虫经过三个幼虫龄期。使用解剖学和发育标记物,我们可以早在第一龄期就进一步区分生殖蚁幼虫、雄蚁幼虫和工蚁幼虫的发育。总的来说,我们希望我们在这里呈现的个体发生系列将成为未来蚂蚁发育表的蓝图。