Coupled Genomic Evolutionary Histories as Signatures of Organismal Innovations in Cephalopods

Abstract

How genomic innovation translates into organismal organization remains largely unanswered. Possessing the largest invertebrate nervous system, in conjunction with many species-specific organs, coleoid cephalopods (octopuses, squids, cuttlefishes) provide exciting model systems to investigate how organismal novelties evolve. However, dissecting these processes requires novel approaches that enable deeper interrogation of genome evolution. Here, the existence of specific sets of genomic co-evolutionary signatures between expanded gene families, genome reorganization, and novel genes is posited. It is reasoned that their co-evolution has contributed to the complex organization of cephalopod nervous systems and the emergence of ecologically unique organs. In the course of reviewing this field, how the first cephalopod genomic studies have begun to shed light on the molecular underpinnings of morphological novelty is illustrated and their impact on directing future research is described. It is argued that the application and evolutionary profiling of evolutionary signatures from these studies will help identify and dissect the organismal principles of cephalopod innovations. By providing specific examples, the implications of this approach both within and beyond cephalopod biology are discussed.

Emergence of novel genomic regulatory regions associated with light-organ development in the bobtail squid

“…The genomic changes associated with the origin and evolution of novel organs are often difficult to discern, as there are several paths to generate complex gene regulation, including, but not limited to: novel genes, gene duplication, and evolution of noncoding regulatory elements. 5 A recent genomic study 17 pointed to divergent modes of symbiotic organ evolution in the bobtail squid. Of interest, the light organ, which is present only in some species of the squid lineages, did not show any transcriptomic evidence of duplicated gene families or novel genes.…”

“…The coleoid cephalopod clade, emerging around 400 million years ago (mya), 1 , 2 (octopus, squid, cuttlefish) possesses the largest invertebrate nervous system, a feature associated with extensive behavioral and camouflage abilities. 3 , 4 Although certain genomic features have been associated with morphological innovations in cephalopods, 5 because of the large genetic distances between cephalopods and other mollusks, as well as the lack of regulatory genomic data in this group; it has been challenging to identify and reconstruct the genomic innovations within this clade. Only recently, potential links between large-scale genomic rearrangements in the coleoid ancestor and organismal novelties 6 , 7 , 8 were uncovered.…”

Incorporating evolutionary based tools in cephalopod fisheries management

“…Nevertheless, phenotypic plasticity does not preclude genomic evolution-in nature those processes often go hand by hand, and in terms of affecting the evolutionary trajectories they interact in multiple ways (Pfennig et al 2010). The important role of environmental selection in shaping the cephalopod genomic and phenotypic variability at larger evolutionary scale cannot be disputed (Lindgren et al 2012;Ritschard et al 2019). Heritability estimate of a trait provides information on the relative contribution of direct environmental vs. genetic effects to the phenotypic variance, and is usually used to distinguish between plastic and genetically adaptive responses.…”

Beyond “living fossils”: Can comparative genomics finally reveal novelty?

“…Coleoid cephalopods (octopus, squid, and cuttlefish), with their unusually large invertebrate nervous systems, complex behavioural traits, and unique mode of development, provide a rare and perhaps unique test of our ability to understand the evolution of morphological novelty at the genomic level. The initial sampling of coleoid cephalopod genomes revealed a surprisingly clear set of shared genomic features (Ritschard et al, 2019, Albertin & Simakov, 2020). One surprising finding was that their large genomes were not derived from the process of whole‐genome duplication, as in vertebrates – genome size increase in coleoids occurred predominantly via the expansion of repetitive DNA (e.g., transposons).…”