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.

Highlights

  • IntroductionModern ideas about the mechanisms of evolution of eukaryotes are based mostly on Darwin’s theory of natural selection, Kimura’s neutral theory (as well as Ohta’s “nearly neutral” theory), and a set of gene transmission rules [1,2]

  • Modern ideas about the mechanisms of evolution of eukaryotes are based mostly on Darwin’s theory of natural selection, Kimura’s neutral theory, and a set of gene transmission rules [1,2]

  • Similar to M. lignano and M. janickei, our findings suggest that M. mirumnovem arose via whole genome duplication (WGD) followed by considerable chromosome reshuffling

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Summary

Introduction

Modern ideas about the mechanisms of evolution of eukaryotes are based mostly on Darwin’s theory of natural selection, Kimura’s neutral theory (as well as Ohta’s “nearly neutral” theory), and a set of gene transmission rules [1,2]. The gradual accumulation of mutations (deleterious, neutral, or advantageous) followed by natural selection and genetic drift is considered the main mechanism underlying the gradual evolution of most life forms. At the evolutionary origin of vertebrates, there were two WGD events, with additional events occurring among some groups of teleost fishes (e.g., the family Salmonidae experienced two more rounds of WGD) [15] Most of these WGD events were probably associated with autopolyploidy, but in the genome evolution of some representatives of fishes (for instance, the goldfish Carassius auratus), amphibians (African clawed frog Xenopus laevis), and reptiles (Ambystoma salamanders), WGDs took place after interspecific hybridization [16,17,18,19]. The genomes and karyotypes of such allopolyploids were observed to be less stable compared to autopolyploids and were usually found to be significantly reorganized [16,17,23]

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