Special topic on EvoDevo: emerging models and perspectives

Communication between developmental and evolutionary scientists has historically been a challenge, with their respective foci being molecular mechanisms during the development of an individual and long-term shifts in allele frequency in populations. Yet, uniting these perspectives provides a better understanding of biological functions. Ernst Haeckel's biogenetic argument that, "ontogeny recapitulates phylogeny, " offers us with an early glimpse at how useful such a synthesis of evolution and development (EvoDevo) can be. Furthermore, the recently emerging developmental and evolutionary techniques make it possible to establish and explore new model organisms in greater depth (Zhao et al. 2021). These techniques bridge and connect these two fields together and extend the developmental questions to evolutionary field and vice versa.

In recent years, the biology community has made significant strides in merging the exciting field of evolution and development. To showcase newly achieved progresses and the advances of EvoDevo on the understanding of biology, Marine Life Science & Technology (MLST) presents a special issue featuring 11 research articles and two reviews. These contributions span model and non-model organisms, exploring individual behavior, organ morphology, and cellular activities at DNA, RNA, and protein levels. Techniques, such as amplicon library preparation, omics sequencing, RNAi gene knockdown in non-model organisms, and comprehensive genetic/developmental toolkits, are also covered. Topics range from organ development and evolution to developmental switches in life history stages, RNA degradation, post-translational modifications, transcription factors in cellular responses, the role of chemokines in fish reproduction, pattern formation, the impact of the immune system on regeneration, and molecular mechanisms underlying antibiotic-induced mutagenesis. Join us in delving into these fascinating insights that bridge the gap between development and evolution. Below, we offer a brief summary of each paper.

Teleosts employ various reproduction methods, some of which are notably distinctive. For example, over 300 Syngnathidae species (seahorses, pipefishes, and sea dragons) exhibit male pregnancies with specialized interfaces between the parent and the brood; e.g., brood pouches providing protection, nourishment, and oxygen regulation. It is known that chemokines are crucial in mammalian maternal–fetal interfaces, while their roles in fish reproduction are unclear. Jiang et al. (2023) examined chemokine genes in 22 Syngnathidae fish species, each of which represents different reproductive modes, revealing variations in gene copy numbers and evolutionary rates. Syngnathidae lost cxcl13 and cxcr5 involved in lymphoid organ development but showed unique mutations in cxcl12b and ccl44, suggesting immune functions during gestation. Transcriptome analysis indicated diverse chemokine expression in different brood pouch types, suggesting adaptive variations. Challenge experiments supported the joint immune function of chemokine genes during male pregnancy, shedding light on the evolutionary diversity of fish chemokine genes in various reproductive modes.

Gli transcription factors serve as key components within the Hedgehog (Hh) signaling pathway, governing complex cellular responses contingent upon Hh concentration. Huang et al. (2023) present findings on Gil in an early chordate (amphioxus), which possesses a single Gli gene producing two isoforms, GliS and GliL, through alternative splicing. Knocking out Gli in amphioxus revealed significant defects in left–right asymmetry development, resembling the effects seen in Hh mutants. Importantly, the deletion of GliL had no discernible impact on neural tube patterning, while complete Gli knockout only affected the expression of Olig family genes. These disparities hint at distinct functions for amphioxus Gli isoforms, thereby shedding light on the complexity of Hh signaling and its evolutionary origins.

Mollusca, the second-largest animal phylum, comprises over 100, 000 species across eight classes. Among them, chitons, represented by 1000 species in the class Polyplacophora, exhibit a unique mix of constrained and divergent morphologies, with some possessing remarkable "shell eyes". These shell eyes, complete with lenses and retinas, have sparked scientific intrigue. The phylogeny of major chiton clades is well-established, except for one critical lineage: Schizochiton. Liu et al. (2023) sequenced the genome of Schizochiton incisus and analyzed transcriptome data from other polyplacophorans, unveiling a robust phylogenetic relationship. They found that Schizochitonoidea is the sister group to other Chitonoidea in Chitonina, suggesting that shell eyes originated in Schizochitonoidea and were later acquired by other genera in Chitonoidea. This study not only clarifies the evolutionary history of chitons but also provides insights into the broader evolution of Polyplacophora.

The organizer plays a vital role in establishing the dorsal–ventral axis and mesodermal development during embryogenesis, yet the full comprehension of the molecules associated with this process remains elusive, despite a grasp of the signaling mechanisms. In a breakthrough using the mollusk Lottia peitaihoensis, Tan et al. (2023) demonstrated that the inhibition of the fibroblast growth factor receptor (FGFR) with SU5402 leads to a compromised organizer specification. This disruption affects the bone morphogenetic protein (BMP) signaling gradient and dorsal–ventral patterning, highlighting the regulatory function of FGFR in shaping the organizer's role. Importantly, the study identifies varying sensitivities of distinct aspects of organizer function to FGFR/MAPK signaling, enhancing our understanding of spiralian organizers.

Marine invertebrates often transition from planktonic larvae to benthic spats through settlement and metamorphosis, i.e., indirect development. Understanding metamorphosis aids us in unraveling the evolution of indirect development. Despite previous studies on the environmental, microbial, and neurohormonal aspects of metamorphosis, gene regulation network (GRN) dynamics have remained largely unexplored. Xu et al. (2023) focus on pediveliger larvae of the Pacific oyster Crassostrea gigas, revealing distinct gene regulation networks before, during, and after metamorphosis. Upregulation of genes related to membrane-integrated receptors and nervous system remodeling precedes metamorphosis initiation. Metamorphosis itself involves a burst of biogenesis, including enzymes and structural proteins, suggesting extensive protein synthesis. Complex GRNs involving transcription factors like homeobox, basic helix-loop-helix, and nuclear receptors are observed, suggesting an ancient role of nuclear receptor regulation in animal metamorphosis. This study sheds light on the intricate genetic dynamics underlying metamorphosis in marine invertebrates.

Antibiotic-resistant bacteria pose a significant threat to human health. Understanding how resistance emerges is crucial. This study delves into the origins of antibiotic-induced mutations, focusing on fluoroquinolones. These antibiotics elevate mutation rates through the SOS response pathway and DNA repair system inefficiencies. Lin et al. (2023b) reveal that the SOS response contributes significantly, accounting for 30–50% of base-pair substitution mutations when exposed to sub-lethal fluoroquinolone levels. The SOS response also influences transversions, structural variations, and mutation spectrum. Meanwhile, DNA repair systems reduce base-pair substitution and transversion rates but increase structural variation. These findings provide a quantitative breakdown of how the SOS response and DNA repair systems contribute to antibiotic-induced mutagenesis, advancing our understanding of antibiotic resistance development.

Evolution and development of the chambered heart has played a critical role in changes of circulatory system efficiency. Lu et al. (2023) have focused on mollusks, specifically comparing the hearts of a model snail and a model scallop, to understand the genetic basis behind the evolution of cardiac chambers. They highlight differences and similarities related to the structure and organization of heart chambers between the two models. They then delve deeper and address the underlying regulatory network through RNA sequencing. This research provides novel insights into the evolution of cardiac chambers.

Exogenous RNA poses a constant threat to genome stability, but cells have mechanisms to deal with this, including RNA degradation and RNA-mediated silencing. RNA interference (RNAi) is a key defense mechanism and a powerful gene manipulation tool. To optimize RNAi, there is a need to understand how cells recognize and eliminate foreign RNA, especially the entry, intracellular transport, and immune responses. Tang et al. (2023) review recent progress in these areas and highlight their potential for improving RNA delivery methods, promising advancements in both defense against exogenous RNA and biotechnological applications.

Green algae, with their long evolutionary history, thrive in diverse environments, including polar regions. Zhang et al. (2023c) isolated Microglena sp. YARC, a psychrophilic green alga from Antarctic sea ice. They found that over the last 37–48 million years, there has been a significant increase in its gene count, and this coincided with the formation of the Southern Ocean. Duplicated genes were enriched in photosynthesis, DNA repair, and fatty acid metabolism pathways. Unique Microglena-specific gene families, including collagen-like proteins, were identified. This study highlights how gene duplication and functional innovation play a role in the adaptation of polar algae to extreme and colder polar environments.

Multicellularity stands as a major milestone in the course of evolution, with cell–cell adhesion serving as a fundamental mechanism facilitating this transition. In the context of epithelial tissues, cell–cell adhesion hinges on the formation of E-cadherin–catenin complexes, which constitute the basis for adherens junctions. The review by Zhang et al. (2023a) summarizes how advances have revealed the dynamics and interactions of these complexes with E-cadherin superclusters, actomyosin, and cortical mechanics. The nanoscale architecture of these complexes adapts to junctional tension, impacting mechano-transduction by strengthening or weakening specific interactions. While post-translational modifications like phosphorylation and glycosylation play a role, their precise functions remain unclear. This overview focuses on nanoscale architectures and post-translational modifications of E-cadherin complexes, drawing from recent in vivo studies and computational modeling to deepen our understanding of their role in epithelial cell and tissue morphogenesis.

Amplicon sequencing has become a powerful tool in EvoDevo research, facilitating the targeted exploration of specific genes within diverse cells or species within a community. However, current amplicon library preparation methods, when applied to a large number of samples, impose significant financial and time constraints, and are usually limited to a handful of well-established gene markers. To solve this problem, Ni et al. (2023) introduce an efficient one-step PCR amplicon library construction protocol (OSPALC). This approach, tested on mock bacterial communities and environmental samples, delivered high-quality reads for species identification. OSPALC requires just one regular PCR with long primers, reducing costs to 7% of those currently required for multi-step PCR methods. They demonstrate its application for 16S rDNA V4 regions and offer tools for designing primers targeting any genomic regions. OSPALC is a game-changer for diverse research fields.

Freshwater fish trypanosomes, economically significant parasites, have typically been classified based on subjective criteria, such as cell morphology and host species. Zhang et al. (2023b) provide improved methods, using detailed phylogenetic and haplotype diversity analysis of trypanasome 18S rRNA genes, including new sequences from Trypanosoma carassii and T. danilewskyi. By achieving a 99.5% sequence similarity, they identify 15 operational taxonomic units and propose three scenarios for distinguishing T. carassii from other aquatic trypanosomes. The research suggests the existence of a limited number of freshwater fish trypanosomes, with T. carassii showing the broadest geographical and host range. These findings support the idea of an umbrella complex comprising T. carassii and two closely related species, shedding new light on their phylogeny-based classification.

Styela clava, a globally distributed ascidian, is a useful model for evolutionary and developmental biology. However, existing developmental resources and molecular manipulation tools for this species are lacking. Lin et al. (2023a) help to fill this gap by establishing a developmental atlas and a web-based image resource from fertilized eggs to hatching larvae, using confocal laser microscopy and 3D reconstruction techniques. Notably, the study reveals unique notochord cell behaviors in S. clava embryos, offering a valuable comparative model for tissue morphogenesis research. A chemical-washing method was also developed for easy chorion removal, enabling transgenic manipulation through electroporation and tissue-specific fluorescent labeling. These innovations provide a powerful toolkit for investigating embryogenesis and evolution using S. clava as a model organism.

This special issue, while relatively concise in its coverage of the EvoDevo topic, merits our sincere appreciation for the authors and reviewers for their dedicated contributions. We extend our gratitude to the Editor-in-Chief Prof. Weibo Song, who diligently oversaw all the submissions and guided the review processes. We are confident that these studies provide invaluable insights into the field of EvoDevo, particularly concerning the establishment of new marine model organisms and address diverse aspects, such as organ morphogenesis and evolution, as well as genetic variation and environmental adaptation.

Acknowledgements

This work was supported by the Science & Technology Innovation Project of Laoshan Laboratory (No. LSKJ202203204).

Author contributions

HL and BD wrote and revised this manuscript.

Data availability

No original data were generated in this manuscript.

Declarations

Conflict of interest

Authors Hongan Long and Bo Dong are members of the Editorial Board, but they were not involved in the review of or decision related to this manuscript.

Animal and human rights statement

Not applicable.