Indoles induce metamorphosis in a broad diversity of jellyfish, but not in a crown jelly (Coronatae)

Many animals go through one or more metamorphoses during their lives, however, the molecular underpinnings of metamorphosis across diverse species are not well understood. Medusozoa (Cnidaria) is a clade of animals with complex life cycles, these life cycles can include a polyp stage that metamorphoses into a medusa (jellyfish). Medusae are produced through a variety of different developmental mechanisms—in some species polyps bud medusae (Hydrozoa), in others medusae are formed through polyp fission (Scyphozoa), while in others medusae are formed through direct transformation of the polyp (Cubozoa). To better understand the molecular mechanisms that may coordinate these different forms of metamorphosis, we tested two compounds first identified to induce metamorphosis in the moon jellyfish Aurelia aurita (indomethacin and 5-methoxy-2-methylindole) on a broad diversity of medusozoan polyps. We discovered that indole-containing compounds trigger metamorphosis across a broad diversity of species. All tested discomedusan polyps metamorphosed in the presence of both compounds, including species representatives of several major lineages within the clade (Pelagiidae, Cyaneidae, both clades of Rhizostomeae). In a cubozoan, low levels of 5-methoxy-2-methylindole reliably induced complete and healthy metamorphosis. In contrast, neither compound induced medusa metamorphosis in a coronate scyphozoan, or medusa production in either hydrozoan tested. Our results support the hypothesis that metamorphosis is mediated by a conserved induction pathway within discomedusan scyphozoans, and possibly cubozoans. However, failure of these compounds to induce metamorphosis in a coronate suggests this induction mechanism may have been lost in this clade, or is convergent between Scyphozoa and Cubozoa.诸多动物在生命周期中会经历一次或多次变态发育，但目前学界对不同类群动物变态发育的分子基础仍缺乏深入认知。刺胞动物门（Cnidaria）下的水母亚门（Medusozoa）是一类具有复杂生活史的动物类群，其生活史通常包含水螅体（polyp）变态为水母体（medusa，俗称水母）的阶段。水母体的产生存在多种发育路径：部分水螅纲（Hydrozoa）物种的水螅体可通过出芽方式产生水母体；部分钵水母纲（Scyphozoa）物种通过水螅体分裂形成水母体；还有部分立方水母纲（Cubozoa）物种则通过水螅体直接转化生成水母体。为深入解析调控这类多样变态发育模式的分子机制，我们以涵盖广泛类群的水母亚门水螅体为实验材料，测试了两种最初在海月水母（Aurelia aurita）中被证实可诱导变态发育的化合物：吲哚美辛（indomethacin）与5-甲氧基-2-甲基吲哚（5-methoxy-2-methylindole）。本研究发现，含吲哚结构的化合物可在多个类群的物种中诱导变态发育。所有受试的盘水母亚目（Discomedusae）水螅体在两种化合物的作用下均发生了完全变态发育，涵盖该演化支下多个主要类群的代表物种：包括旗口水母科（Pelagiidae）、霞水母科（Cyaneidae）以及根口水母目（Rhizostomeae）的两个演化支。在受试的立方水母纲物种中，低浓度的5-甲氧基-2-甲基吲哚可稳定诱导其完成健康的变态发育。与之相反，两种化合物均无法诱导受试冠水母目（Coronatae）钵水母发生水母体变态发育，也无法促使受试的两种水螅纲物种产生水母体。本研究结果支持如下假说：盘水母亚目钵水母乃至立方水母纲的变态发育，可能由一条保守的诱导通路所介导。但这两种化合物无法诱导冠水母类发生变态发育，这提示该诱导机制可能在冠水母类演化支中发生了次生丢失，或是钵水母纲与立方水母纲的该诱导机制为趋同演化而来。