Multiple developmental pathways in organisms with developmentally complex life cycles

Abstract

One aspect under which an organism's life cycle can be considered complex is when the very same organism can undertake, or obligatorily undertakes, multiple developmental pathways. Examples are organisms with alternation of generations, like most plants, or organisms with reproductive and/or developmental options, like many marine invertebrates. With a broad taxonomic coverage across the eukaryotes, we survey these developmentally complex life cycles, presenting selected case studies to illustrate the relationships between the diverse developmental pathways within the same organism for what concerns morphogenesis and gene expression. We highlight the deep connections between the different types of cycles and show their relationship with phenotypic plasticity, sexual dimorphism and ecological adaptation. The collected materials and organized concepts can provide the basis for future investigations on the disparity of complex life cycles and their evolution across the tree of life.

Keywords: alternation of generations; asexual reproduction; gene expression; morphogenesis; parthenogenesis; plasticity; regeneration; sexual reproduction.

FIGURE 1

The different ways a life cycle can present developmental complexity. Thick arrows are developmental pathways, thin arrows connect parents to offspring through reproduction. (a) Monogenerational life cycle where individual development includes profound phenotypic transformations (e.g., holometabolous insects). (b) Monogenerational life cycle where alternative (facultative) options for development can be taken, so that developmental processes first diverge and then converge again in a subsequent stage (e.g., some nematodes). (c) Monogenerational life cycle where alternative (facultative) options for reproduction (e.g., sexual, asexual) can be taken, so that developmental processes have a different start and pathway (e.g., many plants). (d) Multigenerational life cycle where the cycle obligatorily passes through more than one organizational form, each with its development and reproduction (e.g., medusozoan cnidarians). Combinations of the four kinds of complexity and further developmental complications are possible. Circle, young: square, adult; do, developmental option; dp, developmental phase; g, generation; ro, reproductive option; R, reproduction.

FIGURE 2

Schematic representation of the life cycle of the nematode Caenorhabditis elegans, highlighting the two alternative developmental options (different tones of blue). Pink arrow, sexual reproduction; light and dark blue arrows, development.

FIGURE 3

Schematic representation of the life cycle of the angiosperm Kalanchoe pinnata, highlighting the two alternative developmental options, upon sexual or asexual reproduction (different tones of blue). Pink arrow, sexual reproduction; red arrow, asexual reproduction; light and dark blue arrows, development. Figure not to scale.

FIGURE 4

Schematic representation of the life cycle of the moss Physcomitrium patens, highlighting the two types of generation, gametophyte and sporophyte (different tones of blue). Pink arrows, sexual reproduction (meiosis and karyogamy); red arrow, asexual reproduction; light and dark blue arrows, development. Figure not to scale.

FIGURE 5

Schematic representation of the life cycle of the cnidarian Clytia hemisphaerica, highlighting the two generations, polyp and medusa (different tones of blue). Pink arrow, sexual reproduction; red arrows, asexual reproduction; light and dark blue arrows, development. Figure not to scale.

FIGURE 6

Schematic representation of the life cycle of the aphid Acyrthosiphon pisum, highlighting the two types of generation, amphigonic and parthenogenetic (different tones of blue). Pink arrow, amphigonic reproduction; red arrows, parthenogenetic reproduction; light and dark blue arrows, development. Figure not to scale.

FIGURE 7

Schematic representation of the life cycle of the tunicate Botryllus schlosseri, highlighting the two types of generation, solitary and colonial (different tones of blue). Pink arrow, sexual reproduction; red arrows, asexual reproduction; light and dark blue arrows, development. Figure not to scale.

FIGURE 8

Schematic representation of the life cycle of the cellular slime mould Dictyostelium discoideum, highlighting the two types of generation, unicellular and multicellular (different tones of blue). Pink arrow, sexual reproduction; red arrows, asexual reproduction; light and dark blue arrows, development. Figure not to scale.