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Sci Rep
2022 Dec 10;121:21408. doi: 10.1038/s41598-022-26059-4.
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Trioecy is maintained as a time-stable mating system in the pink sea urchin Toxopneustes roseus from the Mexican Pacific.
Díaz-Martínez JP, Mejía-Gutiérrez LM, Islas-Villanueva V, Benítez-Villalobos F.
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Trioecy is a sexual system that consists of the co-occurrence of females, males and hermaphrodites in a population and is common in plants; however, in animals it is uncommon and poorly understood. In echinoderms, trioecy had never been recorded until now. Frequencies of females, males, and hermaphrodites were evaluated and gametogenic development was histologically characterized in a population of Toxopneustes roseus inhabiting the Mexican Pacific. Trioecy in this population is functional and temporally stable, since the three sexes coexisted in each sampling month. The hermaphrodites presented similar gametogenic development as the females and males and participated during the spawning season, contributing to the population's reproductive process. Trioecy is considered an evolutionarily transitory state, and it is extremely difficult to explain its presence in a species. We hypothesize that continuous ocean warming represents a threat to the survival of this population of T. roseus, since its early developmental stages, which represent a population bottleneck, are more vulnerable to high temperatures than other sea urchins inhabiting the area, while its population density is significantly lower. These conditions generate a strongly stressed environment, which is the determining factor that maintains the stability of trioecy in the species in which it has been studied.
Figure 1. Location of the study area showing the position of Playa Tijera. The map in this figure was created with ArcMap Desktop (Version 10.8), https://desktop.arcgis.com/es/arcmap.
Figure 2. Frequency of sexes (%) of T. roseus during the sampling period. The asterisk indicates the month in which hermaphroditic individuals were not found.
Figure 3. Gonad section of specimens with the presence of hermaphroditism, (A) gonad section with a larger presence of male gametes, (B) gonad section with a larger presence of oocytes, and (C) gonad with a similar proportion of both gametes. Gw gonad wall, L lumen, Mo mature oocytes, Ms mature spermatozoa, No nucleolus, Np nutritive phagocytes, O oocytes, Og oogonia, Pvo previtellogenic oocytes, S spermatids, Vo vitellogenic oocytes. Scale bars are 100 µm.
Figure 4. Relative frequencies of the reproductive stages of Topxopneustes roseus throughout the sampling period, (A) females, (B) males, and (C) hermaphrodites.
Figure 5. Stages of gametogenic development in hermaphrodites of T. roseus: (A,B) growth stage, (C) maturation stage, (D) spawning stage. Gw gonad wall, L lumen, Mo mature oocytes, Ms mature spermatozoa, N nucleus, No nucleolus, Np nutritive phagocytes, Og oogonia, Pvo previtellogenic oocytes, Ro remaining oocytes, Sc spermatogenic columns, Sg Spermatogonia, Vo vitellogenic oocytes. The asterisk indicates empty spaces due to the release of gametes. Scale bars are 100 µm.
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