Unraveling the origin of Cladocera by identifying heterochrony in the developmental sequences of Branchiopoda

Abstract

IntroductionOne of the most interesting riddles within crustaceans is the origin of Cladocera (water fleas). Cladocerans are morphologically diverse and in terms of size and body segmentation differ considerably from other branchiopod taxa (Anostraca, Notostraca, Laevicaudata, Spinicaudata and Cyclestherida). In 1876, the famous zoologist Carl Claus proposed with regard to their origin that cladocerans might have evolved from a precociously maturing larva of a clam shrimp-like ancestor which was able to reproduce at this early stage of development. In order to shed light on this shift in organogenesis and to identify (potential) changes in the chronology of development (heterochrony), we investigated the external and internal development of the ctenopod Penilia avirostris and compared it to development in representatives of Anostraca, Notostraca, Laevicaudata, Spinicaudata and Cyclestherida. The development of the nervous system was investigated using immunohistochemical labeling and confocal microscopy. External morphological development was followed using a scanning electron microscope and confocal microscopy to detect the autofluorescence of the external cuticle.ResultsIn Anostraca, Notostraca, Laevicaudata and Spinicaudata development is indirect and a free-swimming nauplius hatches from resting eggs. In contrast, development in Cyclestherida and Cladocera, in which non-swimming embryo-like larvae hatch from subitaneous eggs (without a resting phase) is defined herein as pseudo-direct and differs considerably from that of the other groups. Both external and internal development in Anostraca, Notostraca, Laevicaudata and Spinicaudata is directed from anterior to posterior, whereas in Cyclestherida and Cladocera differentiation is more synchronous.ConclusionsIn this study, developmental sequences from representatives of all branchiopod taxa are compared and analyzed using a Parsimov event-pairing approach. The analysis reveals clear evolutionary transformations towards Cladocera and the node of Cladoceromorpha which correspond to distinct heterochronous signals and indicate that the evolution of Cladocera was a stepwise process. A switch from a strategy of indirect development to one of pseudo-direct development was followed by a shift in a number of morphological events to an earlier point in ontogenesis and simultaneously by a reduction in the number of pre-metamorphosis molts. A compression of the larval phase as well as a shortening of the juvenile phase finally leads to a precocious maturation and is considered as a gradual progenetic process.

Neuroanatomy of the optic ganglia and central brain of the water flea Daphnia magna (Crustacea, Cladocera)

“…This fusion in the optic system varies throughout several taxa of the Branchiopoda. A single Bcyclopean^eye is present in all cladocerans (e.g., Fritsch et al 2013;Kirsch and Richter 2007) and in members of their cyclestheridan sister group, thus showing their close relationship (Fritsch et al 2013;Fritsch and Richter 2012;Olesen et al 1996). Despite the fused eyes, the degree of fusion of the optic ganglia varies among the cladocerans (Hanström 1928;Kirsch and Richter 2007;Leder 1915), and these arise from separate anlagen early in development (Threlkeld 1979;Ungerer et al 2011).…”

“…Despite the fused eyes, the degree of fusion of the optic ganglia varies among the cladocerans (Hanström 1928;Kirsch and Richter 2007;Leder 1915), and these arise from separate anlagen early in development (Threlkeld 1979;Ungerer et al 2011). In other branchiopods, the compound eyes are positioned very close to each other, as, e.g., in Triops and Lepidurus (Notostraca) (Fritsch et al 2013;Fritsch and Richter 2010;Harzsch and Walossek 2001).…”

EvoDevo and Its Significance for Animal Evolution and Phylogeny

“…Patterns of heterochrony may contain useful phylogenetic signal, as demonstrated by, e.g., Guralnick and Lindberg ( 2001 ), who produced a phylogenetic tree of several lophotrochozoan taxa based on the timing of cell lineage events and found that the phylogenetic hypothesis thus obtained replicated patterns found in more traditional analyses. In another study, patterns of heterochrony in the developmental sequences of Branchiopoda were used to identify the origin of Cladocera (Fritsch et al 2013 ).…”

Research Trends in Cladoceran Diversity from Kashmir Himalaya

“…It was Carl Claus in 1876, who claimed that cladocerans [3] had evolved from free-swimming 'conchostracan' larvae (clam shrimps). Among the Branchiopoda, Cladocera encompasses the morphologically most diverse group [3].…”

“…It was Carl Claus in 1876, who claimed that cladocerans [3] had evolved from free-swimming 'conchostracan' larvae (clam shrimps). Among the Branchiopoda, Cladocera encompasses the morphologically most diverse group [3]. Cladocera are commonly known as 'water fleas' due to their jerky swimming movements facilitated by their paired second antennae [4].…”