microRNAs as Indicators into the Causes and Consequences of Whole Genome Duplication Events

Abstract

Whole genome duplications (WGDs) have long been considered the causal mechanism underlying the dramatic increase in vertebrate morphological complexity relative to invertebrates. This is due to the retention and neo-functionalization of paralogues generated during these events, evolving new regulatory circuits, and ultimately morphological novelty. Nonetheless, an alternative hypothesis suggests that behind the retention of most paralogues is not neo-functionalization, but instead the degree of the inter-connectivity of the intended gene product, as well as the mode of the WGD itself. Here, we explore both the causes and consequences of WGD by examining the distribution, expression, and molecular evolution of microRNAs (miRNAs) in both gnathostome vertebrates as well as chelicerate arthropods. We find that although the number of miRNA paralogues tracks the number of WGDs experienced within the lineage, few of these paralogues experienced changes to the seed sequence, and thus are functionally equivalent relative to their mRNA targets. Nonetheless, the paralogues generated by the gnathostome 2R allotetraploidization event are retained in higher numbers on one sub-genome relative the second, with the miRNAs found on the preferred set of paralogons showing both higher expression of mature miRNA transcripts and slower molecular evolution of the precursor miRNA sequences. Importantly, WGDs do not result in the creation of miRNA novelty, nor do WGDs correlate to increases in complexity. Instead, it is the number of miRNA seed sequences in the genome itself that not only better correlate to instances in complexification, but also mechanistically explain why complexity increases when new miRNA families are established.

MirGeneDB 2.1: toward a complete sampling of all major animal phyla

“…For the ecdysozoan node, we added five new arthropod species. We included the Atlantic horseshoe crab Limulus polyphemus as well as the Arizona bark scorpion Centruroides sculpturatus as two new chelicerate representatives to better characterize the whole genome duplications events found in these lineages ( 43 ). We also included the crustacean model system Daphnia magna along with two additional Drosophila species, D. simulans and D. yakuba .…”

“…This did not affect their nomenclature, only the assigned phylogenetic origin. However, taking advantage of recent insights into the whole genome duplication (WGD) events early in gnathostome history, numerous name changes were also made to reflect the origin of suites of microRNA genes ( 43 ). As detailed by Simakov et al.…”

“… MirGeneDB nomenclature system of gnathostome microRNA genes. ( A ) Model of vertebrate genome evolution adapted from ( 43 ). The diploid state of an early chordate ancestor doubled in content (G1) through an autotetraploidy event ( 38 ) generating a tetraploid genome.…”

Rapid Adaptation of Cellular Metabolic Rate to the MicroRNA Complements of Mammals and its Relevance to the Evolution of Endothermy

“…However, these omissions were clearly technical artifacts, since losses of microRNA families have rarely been observed in well-annotated repertoires (Tarver et al, 2018). We and others have recently successfully employed MirGeneDB complements in a range of comparative (Fromm et al, 2021;Hu et al, 2021), phylogenetic (Ma et al, 2021;Rosani et al, 2021), developmental (Taylor et al, 2023;Jenike et al, 2023) and evolutionary studies (Peterson et al, 2022;Zolotarov et al, 2022), as a validation cohort for experimental findings (Kang et al, 2021; Baronti et al, 2020), and as a reference for the development of MirMachine, a novel, machine learning-based bioinformatics tool (Umu et al, 2023).…”

“…However, these omissions were clearly technical artifacts, since losses of microRNA families have rarely been observed in well-annotated repertoires 67 . We and others have recently successfully employed MirGeneDB complements in a range of comparative 99 , phylogenetic 65,100,101 , developmental 80,102,103 and evolutionary studies 104 , as a validation cohort for experimental findings 105,106 , and as a reference for the development of MirMachine, a highly accurate machine learning-based tool for the automatic annotation of microRNA families 107 .…”