Cephalopod-omics: Emerging Fields and Technologies in Cephalopod Biology.

Few animal groups can claim the level of wonder that cephalopods instill in the minds of researchers and the general public. Much of cephalopod biology, however, remains unexplored: the largest invertebrate brain, difficult husbandry conditions, and complex (meta-)genomes, among many other things, have hindered progress in addressing key questions. However, recent technological advancements in sequencing, imaging, and genetic manipulation have opened new avenues for exploring the biology of these extraordinary animals. The cephalopod molecular biology community is thus experiencing a large influx of researchers, emerging from different fields, accelerating the pace of research in this clade. In the first post-pandemic event at the Cephalopod International Advisory Council (CIAC) conference in April 2022, over 40 participants from all over the world met and discussed key challenges and perspectives for current cephalopod molecular biology and evolution. Our particular focus was on the fields of comparative and regulatory genomics, gene manipulation, single-cell transcriptomics, metagenomics, and microbial interactions. This article is a result of this joint effort, summarizing the latest insights from these emerging fields, their bottlenecks, and potential solutions. The article highlights the interdisciplinary nature of the cephalopod-omics community and provides an emphasis on continuous consolidation of efforts and collaboration in this rapidly evolving field.

No evidence for sex chromosomes in natural populations of the cichlid fish Astatotilapia burtoni.

Sex determination (SD) is not conserved among teleost fishes and can even differ between populations of the same species. Across the outstandingly species-rich fish family Cichlidae, more and more SD systems are being discovered. Still, the picture of SD evolution in this group is far from being complete. Lake Tanganyika and its affluent rivers are home to Astatotilapia burtoni, which belongs to the extremely successful East African cichlid lineage Haplochromini. Previously, in different families of an A. burtoni laboratory strain, an XYW system and an XY system have been described. The latter was also found in a second laboratory strain. In a laboratory-reared family descending from a population of the species' southern distribution, a second XY system was discovered. Yet, an analysis of sex chromosomes for the whole species distribution is missing. Here, we examined the genomes of 11 natural populations of A. burtoni, encompassing a wide range of its distribution, for sex-linked regions. We did not detect signs of differentiated sex chromosomes and also not the previously described sex chromosomal systems present in laboratory lines, suggesting different SD systems in the same species under natural and (long-term) artificial conditions. We suggest that SD in A. burtoni is more labile than previously assumed and consists of a combination of non-genetic, polygenic, or poorly differentiated sex chromosomes.

Sex-biased gene expression and recent sex chromosome turnover.

Cichlids are well known for their propensity to radiate generating arrays of morphologically and ecologically diverse species in short evolutionary time. Following this rapid evolutionary pace, cichlids show high rates of sex chromosome turnover. We here studied the evolution of sex-biased gene (SBG) expression in 14 recently diverged taxa of the Lake Tanganyika Tropheini cichlids, which show different XY sex chromosomes. Across species, sex chromosome sequence divergence predates divergence in expression between the sexes. Only one sex chromosome, the oldest, showed signs of demasculinization in gene expression and potentially contribution to the resolution of sexual conflict. SBGs in general showed high rates of turnovers and evolved mostly under drift. Sexual selection did not shape the rapid evolutionary changes of SBGs. Male-biased genes evolved faster than female-biased genes, which seem to be under more phylogenetic constraint. We found a relationship between the degree of sex bias and sequence evolution driven by sequence differences among the sexes. Consistent with other species, strong sex bias towards sex-limited expression contributes to resolving sexual conflict in cichlids. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.

Time matters! Developmental shift in gene expression between the head and the trunk region of the cichlid fish Astatotilapia burtoni.

BACKGROUND: Differential gene expression can be translated into differing phenotypic traits. Especially during embryogenesis, specific gene expression networks regulate the development of different body structures. Cichlid fishes, with their impressive phenotypic diversity and propensity to radiate, are an emerging model system in the genomics era. Here we set out to investigate gene expression throughout development in the well-studied cichlid fish Astatotilapia burtoni, native to Lake Tanganyika and its affluent rivers. RESULTS: Combining RNA-sequencing from different developmental time points as well as integrating adult gene expression data, we constructed a new genome annotation for A. burtoni comprising 103,253 transcripts (stemming from 52,584 genomic loci) as well as a new reference transcriptome set. We compared our transcriptome to the available reference genome, redefining transcripts and adding new annotations. We show that about half of these transcripts have coding potential. We also characterize transcripts that are not present in the genome assembly. Next, using our newly constructed comprehensive reference transcriptome, we characterized differential gene expression through time and showed that gene expression is shifted between different body parts. We constructed a gene expression network that identified connected genes responsible for particular phenotypes and made use of it to focus on genes under potential positive selection in A. burtoni, which were implicated in fin development and vision. CONCLUSIONS: We provide new genomic resources for the cichlid fish Astatotilapia burtoni, which will contribute to its further establishment as a model system. Tracing gene expression through time, we identified gene networks underlying particular functions, which will help to understand the genetic basis of phenotypic diversity in cichlids.