Marine evo-devo: New frontiers from Lophotrochozoa

Oceans cover 71% of the Earth's surface and nurture countless life forms. However, the evolutionary developmental mechanisms of these marine organisms remain poorly understood. Our laboratory recently published a paper titled "Marine evo-devo: New frontiers from Lophotrochozoa" in the international journal The Innovation. By focusing on Lophotrochozoa, one of the most species-rich marine clades, this work offers new perspectives for understanding the origin and diversity of life, unravelling the evolutionary mysteries underlying marine biodiversity.

As an oceanic planet, Earth harbors extraordinary marine biodiversity that provides unique resources for evolutionary studies. However, scientists have long primarily focused on terrestrial model organisms (e.g., fruit flies, mice), overlooking the distinctive value of marine species. The Lophotrochozoa, representing one of the most species-rich marine lineages, encompasses diverse phyla including mollusks (e.g., scallops, octopuses) and annelids (e.g., polychaetes). Their remarkable variations in life cycles and body plans offer an unprecedented opportunity to explore the evolutionary history of life. This review highlights recent breakthroughs and emerging frontiers in marine evo-devo research by focusing on lophotrochozoans, investigating species diversification, life history evolution, organogenesis, and stem cell-mediated regeneration. These findings establish novel conceptual frameworks for understanding the origins and mechanisms of biological diversity.

 Multi-omics Exploration of Lophotrochozoans: Decoding the Evolutionary Code of the Tree of Life

Revolutionizing the marine evo-devo field using cutting-edge omics technologies

Advances in cutting-edge omics technologies and dramatic increases in high-quality genomes and diverse functional genomic data have revolutionized evo-devo understanding. Over the past five years, the number of chromosome-level genomes of lophotrochozoans has increased 21-fold, growing from 11 to 229 species. The explosion of the multi-functional omics data as well as the establishment of comparative multi-omics database have provided invaluable resources and tools for lophotrochozoan genomic research. Strikingly, during the construction and analysis of high-resolution genomic maps, researchers unexpectedly found that they exhibit a slow-evolving pattern with numerous ancestral features, including exceptional preservation of the bilaterian karyotype and a deeply conserved gene repertoire. These unexpected findings provide unique opportunities to gain a deeper understanding of the early origins and evolutionary mechanisms that have shaped animal development. 

Cambrian explosion and the mysterious origin of animal diversity

All major animal phyla appeared suddenly in diverse forms in an event referred to as the “cambrian explosion” (~540 mya). Lophotrochozoans emerged during this significant historical event. Widespread gene family expansions are evident in cambrian animals and play pivotal roles during development, thereby facilitating evolutionary innovations. For example, hox genes have long been a central paradigm in evo-devo body plan evolution studies. In vertebrates, the expression of these genes has been well-documented through the principle of whole-cluster temporal collinearity (WTC). However, this long-standing and fundamental concept has been challenged by broader taxon sampling in lophotrochozoans. A novel pattern, sub-cluster temporal collinearity (STC), was discovered and has since attracted attention. As a “weaker” form of temporal co-linearity, STC may provide crucial insights into the origin and evolutionary mechanisms underlying the dramatic diversification of body plans during the Cambrian Explosion.. 

Life history macroevolution: larva-first or adult-first?

Life cycle strategies have also been proposed as key explanations for species diversity. Many marine animal phyla exhibit indirect development and a ciliated primary larva-bearing biphasic life cycle. However, how metazoan larvae originated remains a major enigma. Historically, the conflicting larva-first and adult-first hypotheses were primarily based on morphological and developmental data, and the "larva-first" hypothesis gaining relatively wider acceptance. These hypotheses are now being discussed again and are combining systematic molecular characterization incorporating lophotrochozoans. Astonishingly, a phylostratigraphic approach has revealed widespread evidence of rapid larval evolution with extraordinary incorporation of novel genes in metazoan species. A hypothesis of a single, ancient metazoan larval intercalation has been proposed. These insights reshape our understanding of the macroevolutionary mechanisms underlying the developmental regulation of primary larvae, both regarding their origin, and how they promote life cycle diversification.

Cephalopod novelties: challenging conventional perceptions

Cephalopods, well known for their sophisticated nervous systems and cognitive capacities, are often marveled at as "alien intelligences" on Earth. Through decoding the octopus genome, researchers found that massive gene family expansions, large-scale genomic rearrangements, and transposable element bursts have led to novel regulatory elements, which may together contribute to their remarkable behavioral plasticity. Besides, the non-synonymous RNA editors, challenge the “iron law” of the central dogma by producing “recoding” results, which are involved in both neural development and neurophysiological functions. Although how cephalopods adopt these unique organismal novelties remain enigmatic, these findings collectively provide a new landscape for elucidating the evolution of developmental strategies across diverse lineages.

Stem cell secrets behind whole-body regeneration

Whole-body regeneration could be the ultimate dream of humanity. Amazingly, this “superpower” is widely found in marine invertebrates, which possess the adult pluripotent stem cells (aPSCs). This contrasts strongly with vertebrates, where the pluripotency of embryonic stem cells gradually diminishes during development. The “indestructible planarian” flatworms, shares approximately 80% of its genes with humans, yet achieves the biological miracle of "immortality" through its remarkable whole-body regenerative capacity. A recent innovative discovery reveals that the embryonic origin of aPSCs is traced to a single lineage (a pair of blastomeres), involving key factors that are crucial for aPSCs’ initial specifications. Understanding the regulation of these powerful stem cells would hold great potential for revealing new biological principles regarding regeneration, and could enlighten therapeutic approaches in regenerative medicine and anti-aging treatments.

Future perspectives: opportunities and challenges

As technological advancements continue to progress, they become powerful allies in the expansion of evo-devo, presenting both new opportunities and challenges. We have foreseen three major trends in future evo-devo studies. First, expanding the research scope to increase phylogenetic coverage remains a top priority. Second, developing systems biology approaches (such as deep learning) presents a promising avenue for functional elucidation of lophotrochozoan genomes, especially for deciphering “dark genes”. Third, sophisticated toolkits for functional investigations of less-established or new emerging model species are pressingly needed, such as planarians, polychaetes, dwarf surf clam, etc. Collectively, it would offer a whole new blueprint for unveiling questions on the nature of animal homology and novelties, informing us links between development and evolution.

DOI:10.1016/j.xinn.2025.100869