Naupliar and Metanaupliar development of Thysanoessa raschii (Malacostraca, Euphausiacea) from Godthåbsfjord, Greenland, with a reinstatement of the ancestral status of the free-living Nauplius in Malacostracan evolution

The presence of a characteristic crustacean larval type, the nauplius, in many crustacean taxa has often been considered one of the few uniting characters of the Crustacea. Within Malacostraca, the largest crustacean group, nauplii are only present in two taxa, Euphauciacea (krill) and Decapoda Dendrobranchiata. The presence of nauplii in these two taxa has traditionally been considered a retained primitive characteristic, but free-living nauplii have also been suggested to have reappeared a couple of times from direct developing ancestors during malacostracan evolution. Based on a re-study of Thysanoessa raschii (Euphausiacea) using preserved material collected in Greenland, we readdress this important controversy in crustacean evolution, and, in the process, redescribe the naupliar and metanaupliar development of T. raschii. In contrast to most previous studies of euphausiid development, we recognize three (not two) naupliar (= ortho-naupliar) stages (N1-N3) followed by a metanauplius (MN). While there are many morphological changes between nauplius 1 and 2 (e.g., appearance of long caudal setae), the changes between nauplius 2 and 3 are few but distinct. They involve the size of some caudal spines (largest in N3) and the setation of the antennal endopod (an extra seta in N3). A wider comparison between free-living nauplii of both Malacostraca and non-Malacostraca revealed similarities between nauplii in many taxa both at the general level (e.g., the gradual development and number of appendages) and at the more detailed level (e.g., unclear segmentation of naupliar appendages, caudal setation, presence of frontal filaments). We recognize these similarities as homologies and therefore suggest that free-living nauplii were part of the ancestral malacostracan type of development. The derived morphology (e.g., lack of feeding structures, no fully formed gut, high content of yolk) of both euphausiid and dendrobranchiate nauplii is evidently related to their non-feeding (lecithotrophic) status

Naupliar and Metanaupliar Development of Thysanoessa raschii (Malacostraca, Euphausiacea) from Godthåbsfjord, Greenland, with a Reinstatement of the Ancestral Status of the Free-Living Nauplius in Malacostracan Evolution.

The presence of a characteristic crustacean larval type, the nauplius, in many crustacean taxa has often been considered one of the few uniting characters of the Crustacea. Within Malacostraca, the largest crustacean group, nauplii are only present in two taxa, Euphauciacea (krill) and Decapoda Dendrobranchiata. The presence of nauplii in these two taxa has traditionally been considered a retained primitive characteristic, but free-living nauplii have also been suggested to have reappeared a couple of times from direct developing ancestors during malacostracan evolution. Based on a re-study of Thysanoessa raschii (Euphausiacea) using preserved material collected in Greenland, we readdress this important controversy in crustacean evolution, and, in the process, redescribe the naupliar and metanaupliar development of T. raschii. In contrast to most previous studies of euphausiid development, we recognize three (not two) naupliar (= ortho-naupliar) stages (N1-N3) followed by a metanauplius (MN). While there are many morphological changes between nauplius 1 and 2 (e.g., appearance of long caudal setae), the changes between nauplius 2 and 3 are few but distinct. They involve the size of some caudal spines (largest in N3) and the setation of the antennal endopod (an extra seta in N3). A wider comparison between free-living nauplii of both Malacostraca and non-Malacostraca revealed similarities between nauplii in many taxa both at the general level (e.g., the gradual development and number of appendages) and at the more detailed level (e.g., unclear segmentation of naupliar appendages, caudal setation, presence of frontal filaments). We recognize these similarities as homologies and therefore suggest that free-living nauplii were part of the ancestral malacostracan type of development. The derived morphology (e.g., lack of feeding structures, no fully formed gut, high content of yolk) of both euphausiid and dendrobranchiate nauplii is evidently related to their non-feeding (lecithotrophic) status

Early (= naupliar type) development of two malacostracan taxa and two non-malacostracan.

<p>(A-D) Four naupliar stages of the Cambrian ‘Orsten’ crustacean <i>Rehbachiella kinnekullensis</i> (from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0141955#pone.0141955.ref020" target="_blank">20</a>]). (E-H) Four naupliar type stages of <i>Branchinecta occidentalis</i> (Anostraca) (from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0141955#pone.0141955.ref075" target="_blank">75</a>]). (I-L) Four (out of six) naupliar stages of <i>Metapenaeopsis dalei</i> (Dendrobranchiata Decapoda) (from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0141955#pone.0141955.ref073" target="_blank">73</a>]).</p

Evolution of naupliar development mapped on a simplified phylogeny of the Malacostraca based on several papers providing partly conflicting phylogenetic results [76, 77].

<p>The figure summarizes the idea supported in this paper, that the naupliar type of development seen in two malacostracan taxa, Euphausiacea and dendrobranchiate decapods (A and B), in essence is primitive for malacostracans and retained, but modified, from earlier in evolution (red line). C-H show other examples of the variation in developmental type in Malacostraca, both of taxa with free-living larvae and direct developers. (C) Early embryonic-like stage of <i>Nebalia longicornis</i> (Leptostraca) (from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0141955#pone.0141955.ref078" target="_blank">78</a>]). (D) Antizoea larva (Stomatopoda). (E) Zoea larva (Brachyura). (F) Late development stage of <i>Tulumella unidens</i> (Thermosbaenacea) (from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0141955#pone.0141955.ref014" target="_blank">14</a>]). (G) <i>Praunus inermis</i> (Mysida) (from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0141955#pone.0141955.ref079" target="_blank">79</a>]). (H) <i>Idotea baltica</i> (Isopoda) (material collected in Denmark by JO). (I) Three examples of non-malacostracan taxa with free living nauplii early in their development (Branchiopoda, Copepoda, and the Cambrian <i>Rehbachiella</i>).</p

Nauplius 2 of <i>Thysanoessa raschii</i> (Euphausiacea), scanning electron microscopy (SEM).

<p>(A) Ventral view of whole specimen. (B) Lateral view of whole specimen. (C) Incipient mouth opening (?). (D) Antenna 1, right side. (E) Antenna 2, right side, anterior view. (F) Mandible, right side, anterior view. (G) Antenna 2 and mandible, right side. (H) Caudal setae, ventral view. (I) Caudal seta, left side, posterior view.</p

Metanauplius of <i>Thysanoessa raschii</i> (Euphausiacea), scanning electron microscopy (SEM).

<p>(A) Lateral view of whole specimen. (B) Caudal view of whole specimen. (C) Appendages (mandible, maxilla 1 and 2, thoracopod 1) of right side, lateral view. (D) Appendages (mandible, maxilla 1 and 2, thoracopod 1) of both sides, ventral view. (E) Frontal view showing antennae 1 and frontal filaments. (F) Marginal spines of posterior part of naupliar shield.</p

<i>Thysanoessa raschii</i> (Euphausiacea), adult morphology and map of sampling sites.

<p>(A) Adult morphology of <i>Thysanoessa raschii</i> (Euphausiacea) (photo by permission from Russel Hopcroft). (B, C) Map of Godthåbsfjord, SW Greenland, with sampling stations indicated by black dots and station numbers. The larvae examined in this study originated from station GF8 (arrow on C).</p