Abstract
BackgroundWithin Malacostraca (Crustacea), direct development and development through diverse forms of larvae are found. Recent investigations suggest that larva-related developmental features have undergone heterochronic evolution in Malacostraca. In the light of current phylogenetic hypotheses, the free-swimming nauplius larva was lost in the lineage leading to Malacostraca and evolved convergently in the malacostracan groups Dendrobranchiata and Euphausiacea. Here we reconstruct the evolutionary history of eumalacostracan (Malacostraca without Phyllocarida) development with regard to early appendage morphogenesis, muscle and central nervous system development, and determine the heterochronic transformations involved in changes of ontogenetic mode.ResultsTiming of 33 developmental events from the different tissues was analyzed for six eumalacostracan species (material for Euphausiacea was not available) and one outgroup, using a modified version of Parsimov-based genetic inference (PGi). Our results confirm previous suggestions that the event sequence of nauplius larva development is partly retained in embryogenesis of those species which do not develop such a larva. The ontogenetic mode involving a nauplius larva was likely replaced by direct development in the malacostracan stem lineage. Secondary evolution of the nauplius larva of Dendrobranchiata from this ancestral condition, involved only a very small number of heterochronies, despite the drastic change of life history. In the lineage leading to Peracarida, timing patterns of nauplius-related development were lost. Throughout eumalacostracan evolution, events related to epidermal and neural tissue development were clearly less affected by heterochrony than events related to muscle development.ConclusionsWeak integration between mesodermal and ectodermal development may have allowed timing in muscle formation to be altered independently of ectodermal development. We conclude that heterochrony in muscle development played a crucial role in evolutionary loss and secondary evolution of a nauplius larva in Malacostraca.Electronic supplementary materialThe online version of this article (doi:10.1186/2041-9139-6-4) contains supplementary material, which is available to authorized users.
Highlights
Within Malacostraca (Crustacea), direct development and development through diverse forms of larvae are found
Recorded events Event sequences were assembled for A. franciscana, G. falcatus, S. ingentis, N. heteropoda, P. fallax forma virginalis, N. integer, and P. hawaiensis by combination of our previous descriptions, literature data, and new observations presented here
Tracing the evolutionary history of eumalacostracan, developmental timing by Parsimov-based genetic inference (PGi) in our study showed that the different tissue types have taken different evolutionary paths depending on the germ layer they originate from
Summary
Within Malacostraca (Crustacea), direct development and development through diverse forms of larvae are found. Comparatively few investigations focus on heterochrony in invertebrate evolution [12,13,14,15,16] Invertebrates, such as the crustaceans (the potential paraphyly of crustaceans has no impact to our study), display an enormous disparity in development, exemplified by the multitude of larval forms and life histories found throughout this group. Despite controversies concerning the phylogenetic relationships within Malacostraca, Dendrobranchiata and Euphausiacea are always placed at nested positions within the tree [24,25,26,27,28,29,30,31,32] In this light, the nauplius larva in Malacostraca has evolved secondarily from ancestors, which either showed direct development or hatched as a more advanced larval stage with a higher number of segments (Figure 1)
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