Integrating Complex Life Cycles in Comparative Developmental Biology

Abstract

The goal of comparative developmental biology is identifying mechanistic differences in embryonic development between different taxa and how these evolutionary changes have led to morphological and organizational differences in adult body plans. Much of this work has focused on direct-developing species in which the adult forms straight from the embryo and embryonic modifications have direct effects on the adult. However, most animal lineages are defined by indirect development, in which the embryo gives rise to a larval body plan and the adult forms by transformation of the larva. Historically, much of our understanding of complex life cycles is viewed through the lenses of ecology and zoology. In this review, we discuss the importance of establishing developmental rather than morphological or ecological criteria for defining developmental mode and explicitly considering the evolutionary implications of incorporating complex life cycles into broad developmental comparisons of embryos across metazoans. Expected final online publication date for the Annual Review of Genetics, Volume 57 is November 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Contrasting the development of larval and adult body plans during the evolution of biphasic lifecycles in sea urchins

“…In organisms with biphasic lifecycles, the switch between the larval and adult body plans does not entirely occur during the brief timeframe of metamorphosis (Formery & Lowe, 2023). Rather, many adult tissues are constructed during larval development, as is the case with the sea urchin rudiment.…”

“…Our data also allow us to address questions about the regulation of adult morphogenesis in sea urchins. It has previously been unclear how organisms with biphasic lifecycles code for two different body plans in the same genome (Formery & Lowe, 2023). Our data suggest that a largely new set of regulatory genes controls the adult developmental process in sea urchins.…”

“…Most metazoan phyla contain species with biphasic lifecycles, also known as indirect development (Formery & Lowe, 2023; Moran, 1994; Nielsen, 2009; Strathmann, 1985; Thorson, 1950). Species that use this life history strategy first develop from embryos into a larval body plan, and then undergo metamorphosis to transition into a separate adult body plan.…”

“…Little is known about how the transition between the larval and adult body plans is regulated at the molecular level. Larval development of phyla such as the hemichordates and annelids is modeled to be controlled by the bilaterian anterior patterning network, while the delayed activation of the trunk patterning network is proposed to initiate adult development (Formery & Lowe, 2023; Gonzalez et al, 2017; Lacalli, 2005; Martin-Zamora et al, 2023).…”

Single-cell transcriptomics reveals evolutionary reconfiguration of embryonic cell fate specification in the sea urchinHeliocidaris erythrogramma

“…Most metazoan life cycles contain intermediate stages that are ecologically distinct from adults. In many clades, this has resulted in the evolution of contrasting anatomical, physiological, and behavioral traits between stages in the life cycle (Garstang 1928; Thorson 1950; Strathmann 1985; Nielsen 1998; Raff and Byrne 2006; Formery and Lowe 2023). Host-specific stages of parasites, insect larvae, amphibians, and diverse marine invertebrates are often so different from adults that they are unrecognizable from the earlier stages of the same life cycle.…”