How the cladoceran heterogonic life cycle evolved—insights from gamogenetic reproduction and direct development in Cyclestherida

Abstract

Here we document the early gamogenetic development of Cyclestherida, including a characterization of the nervous system. Resting eggs in Cyclestheria are protected by an ephippium, built by the major part of the carapace. The first stages of development are enclosed in an outer chorion and an inner vitelline membrane. After shedding of the chorion, the vitelline membrane inflates and later stages are free-floating within the vitelline membrane. Only the juveniles are released from the vitelline membrane. Developmental stages of the gamogenetic direct development and of the parthenogenetic pseudo-direct development are remarkably similar in Cyclestheria, both regarding external and nervous system development. Because of this high degree of correspondence, as well as the important differences to the anamorphic development in Spinicaudata, we suggest that the developmental stages from the gamogenetic life cycle evolved directly from the parthenogenetic life cycle. This implies that resting egg development in Cladoceromorpha does not correspond directly to the resting egg development in large branchiopods. This leads us to the conclusion that the entire heterogonous life cycle in Cladoceromorpha probably evolved anew.

Transitions in functional morphology from “large branchiopods” to Cladocera: Video and confocal microscopic studies of Cyclestheria hislopi (Cyclestherida) and Sida crystallina (Cladocera: Ctenopoda)

“…However, as a whole, an interpretation involving a combination of heterochrony and adaptations to a different lifestyle seems preferable. Cladoceran characters such as the smaller number of trunk limbs (six pairs or less), the smaller number of antennal segments, and the lacking dorsal extension of the trunk limb exopod, are candidates for progenetic traits, because these are also present in embryo‐like (Cyclestherida) and free‐swimming (Spinicaudata) clam shrimp larvae (e.g., Fritsch & Richter, 2015; Olesen, 1999; Olesen & Grygier, 2003, 2004), at least during parts of the larval phase. Other aspects such as the full separation into a locomotory (antennal) and a posterior feeding (trunk limbs) unit, the dominating basal musculature of antennae and trunk limbs, and the lacking separation between endites and endopod in the trunk limbs, do not appear to be of progenetic origin since no particular resemblance to clam shrimp larvae is seen.…”

“…Despite the lack of a detailed understanding of the intermediate evolutionary steps leading to crown‐group Cladocera, it is clear that the modifications eventually involved a full separation into an anterior locomotory antennal system and a specialized posterior filtratory trunk limb system, accompanied by a reduction of limb segmentation and a concentration of musculature proximally. Indeed, these modifications, coupled with a marked shortening of development employing subitaneous eggs and parthenogenesis (see Fritsch et al, 2013; Fritsch & Richter, 2015), are likely the major explanations for the success of the omnipresent Cladocera having conquered both freshwater (and later marine) pelagic water masses and a number of other habitats.…”

“…It was suggested long ago that Cladocera have originated by “neoteny” (now re‐termed progenesis) from clam shrimp‐like ancestors (e.g., Claus, 1876b). In recent years, this theory has been revisited (e.g., Fritsch, Bininda‐Emonds, & Richter, 2013; Fritsch & Richter, 2015; Olesen, 1999; Schminke, 1981) in the light of the now well‐accepted sister group relationship between the clam shrimp Cyclestheria hislopi (Cyclestherida) and Cladocera (Braband, Richter, Hiesel, & Scholtz, 2002; deWaard et al, 2006; Olesen, 1998; Olesen, Martin, & Roessler, 1996; Richter, Olesen, & Wheeler, 2007; Schwentner et al, 2018; Stenderup, Olesen, & Glenner, 2006). Cyclestheria hislopi is an obvious proxy for an ancestral cladoceran‐cyclestheridan (=cladoceromorphan) morphology, sharing both symplesiomorphic character traits with other clam shrimps (e.g., a large bivalved carapace and many serially similar appendages) and synapomorphic character traits with cladocerans (e.g., direct development in dorsal brood chamber and cyclic parthenogenesis).…”

“…It was suggested long ago that Cladocera have originated by "neoteny" (now re-termed progenesis) from clam shrimp-like ancestors (e.g., Claus, 1876b). In recent years, this theory has been revisited (e.g., Fritsch, Bininda-Emonds, & Richter, 2013;Fritsch & Richter, 2015;Olesen, 1999;Schminke, 1981) in the light of the now well-accepted sister group relationship between the clam shrimp Cyclestheria hislopi (Cyclestherida) and Cladocera (Braband, Richter, Hiesel, & Scholtz, 2002;deWaard et al, 2006;Olesen, 1998;Olesen, Martin, & Roessler, 1996;Richter, Olesen, & Wheeler, 2007;Schwentner et al, 2018;Stenderup, Olesen, & Glenner, 2006).…”

The Development of Arthropod Segmentation Across the Embryonic/Post-embryonic Divide – An Evolutionary Perspective

“…It is not always the case that hatching separates embryonic from post-embryonic phases neatly. More or less embryo-like (embryoid) hatchlings are described for many arthropod groups, under a variety of taxon-specific terms (Minelli et al, 2006;Minelli and Fusco, 2013;Fritsch and Richter, 2015;Haug, 2020; Supplementary Table 1).…”