Genome and Karyotype Reorganization after Whole Genome Duplication in Free-Living Flatworms of the Genus Macrostomum

Abstract

The genus Macrostomum represents a diverse group of rhabditophoran flatworms with >200 species occurring around the world. Earlier we uncovered karyotype instability linked to hidden polyploidy in both M. lignano (2n = 8) and its sibling species M. janickei (2n = 10), prompting interest in the karyotype organization of close relatives. In this study, we investigated chromosome organization in two recently described and closely related Macrostomum species, M. mirumnovem and M. cliftonensis, and explored karyotype instability in laboratory lines and cultures of M. lignano (DV1/10, 2n = 10) and M. janickei in more detail. We revealed that three of the four studied species are characterized by karyotype instability, while M. cliftonensis showed a stable 2n = 6 karyotype. Next, we performed comparative cytogenetics of these species using fluorescent in situ hybridization (FISH) with a set of DNA probes (including microdissected DNA probes generated from M. lignano chromosomes, rDNA, and telomeric DNA). To explore the chromosome organization of the unusual 2n = 9 karyotype discovered in M. mirumnovem, we then generated chromosome-specific DNA probes for all chromosomes of this species. Similar to M. lignano and M. janickei, our findings suggest that M. mirumnovem arose via whole genome duplication (WGD) followed by considerable chromosome reshuffling. We discuss possible evolutionary scenarios for the emergence and reorganization of the karyotypes of these Macrostomum species and consider their suitability as promising animal models for studying the mechanisms and regularities of karyotype and genome evolution after a recent WGD.

Large-scale phylogenomics of the genus Macrostomum (Platyhelminthes) reveals cryptic diversity and novel sexual traits

“…Moreover, primarily due to the discovery of a whole-genome duplication and accompanying karyotype instability in M. lignano (Zadesenets et al 2016, 2017), there is increased interest in expanding the genomic resources and molecular phylogenetic placement of additional species in the genus,. To this end, recent work has provided transcriptomic resources for additional species (Brand et al 2020) and field-collections have revealed similar karyological rearrangements to the ones observed in M. lignano in some closely related species, while others were found to have stable diploid genomes (Schärer et al 2020; Zadesenets et al 2020). Accurate phylogenetic information will greatly help guide the search for additional Macrostomum model species and permit to study the (co)evolution of the large diversity of morphological and behavioural traits in the genus, a brief introduction of which we provide in the following.…”

Genome-Wide Characterization of the Nuclear Receptor Gene Family in Macrostomum lignano Imply Its Evolutionary Diversification

“…Besides the SD and TD, the M. lignano-specific hidden tetraploidy may be the main mechanism of this species-specific gene duplication. Recent studies have showed that hidden tetraploidy may occur in the M. lignano genome with ∼75% of the sequence containing repeats and transposon sequences, potentially suggesting wholegenome duplication or more recent large segmental duplications (Wasik et al, 2015;Zadesenets et al, 2017Zadesenets et al, , 2020. Thus, we presume that polyploidy, SD, and TD are the main mechanisms driving the extensive expansion of the NR gene family in M. lignano.…”

The repeatable opportunity for selection differs between pre- and postcopulatory fitness components

“…Deviations from full inheritance of the GFP marker may be due to karyotype polymorphism observed in M. lignano (Zadesenets et al. 2016, 2017, 2020). But here, we used a GFP(+) BAS1 culture in which karyotype polymorphism and heterozygosity was deliberately reduced (Vellnow et al.…”