Expression ofDazlandVasain turtle embryos and ovaries: evidence for inductive specification of germ cells

Abstract

In bilaterian animals, germ cells are specified by the inductive/regulative mode or the predetermined (germ plasm) mode. Among tetrapods, mammals and urodeles use the inductive mode, whereas birds and anurans use the predetermined mode. From histological data it has been predicted that some reptiles including turtles use the inductive mode. Examining turtle oocytes, we find that Dazl RNA, Vasa RNA, and Vasa protein are not localized, suggesting that germ plasm is not present. In turtle embryos at somite stages, primordial germ cells (PGCs) expressing Dazl lie on a path from the lateral posterior extraembryonic endoderm through the gut to the gonad as previously described. In gastrulating embryos, cells expressing Dazl are found in the blastoporal plate and subsequently below the blastoporal plate, indicating that PGCs are generated at the equivalent of the early posterior primitive streak of mammals. Vasa RNA is expressed in somatic cells of gastrula to early somite stages, and Vasa RNA and protein are expressed in PGCs of later embryos. Taken together the evidence strongly suggests that turtles, and other reptiles (lacertoid lizards) with the same location of PGCs in embryos, use the inductive mode of germ cell specification. Phylogenetic analysis of the available evidence supports the following hypotheses: (1) the inductive mode is basal among reptiles, indicating that this mode was maintained as basal tetrapods evolved to amniotes, (2) the predetermined mode arose twice within reptiles, and (3) the induced mode may be used in several lepidosaurs whose PGCs are located in an unusual pattern distributed around the embryo.

Germline development in amniotes: A paradigm shift in primordial germ cell specification

“…In that regard, the embryology of turtles resembles that of mammals and urodele amphibians, and reflects the urodele‐like amniote ancestor, suggesting that the mode of PGC formation could also be conserved (induction). However, the scanty and diverse data available for other reptiles indicates a high degree of variability, in which PGCs are distributed anteriorly, posteriorly or circumferentially at gastrulation, depending on the species 97. Comparative embryology among sauropsids does not help reduce the existing diversity to the binary mode of PGC formation.…”

“…Recently, PGC localization in early stages of development of the turtle Trachemys scripta has been described with the help of molecular markers 97. Dazl and Ddx4 mRNA are expressed both in a structure called the blastopore plate, located posterior to the blastopore supposedly containing prospective mesendoderm cells, and in the lower layer (definitive endoderm or hypoblast) 97, 98, 99.…”

“…Dazl and Ddx4 mRNA are expressed both in a structure called the blastopore plate, located posterior to the blastopore supposedly containing prospective mesendoderm cells, and in the lower layer (definitive endoderm or hypoblast) 97, 98, 99. These expression patterns and the absence of localised RNA for the two germ cell markers in turtle mature oocytes suggests that germ plasm is indeed absent in turtles, and an inductive modality of PGC specification might be employed.…”

“…Moreover, the blastoporal plate region in turtles also expresses Brachyury (as does the mouse primitive streak) 98 and turtle PGCs migrate interstitially to the gonads 97. In that regard, the embryology of turtles resembles that of mammals and urodele amphibians, and reflects the urodele‐like amniote ancestor, suggesting that the mode of PGC formation could also be conserved (induction).…”

Linking a Biological Mechanism to Evolvability

“…One empirical system in which evolvability has been invoked to explain species richness asymmetry in sister clades and differential rates of speciation, has been primordial germ cell (PGC) determination mechanisms [21][22][23][24]. Primordial germ cells are the precursor cells that eventually form eggs and sperm in the developing embryo.…”