Natural Pathways towards Polyploidy in Animals: The <b><i>Squalius alburnoides</i></b> Fish Complex as a Model System to Study Genome Size and Genome Reorganization in Polyploids

Abstract

When comparing the known picture of polyploidy in animals and in plants, it is possible to recognize some similarities, namely: (i) multiple and recurrent origins in several well-established taxonomic groups; (ii) a strong and regular association with hybridization events; (iii) the production of genotypic diversity; (iv) a rapid genomic reshuffling; (v) a very active role of transposable elements in allopolyploids; (vi) a comparatively privileged occurrence in harsher environments when compared with their diploid relatives, and (vii) gene silencing and divergence of duplicated genes without disruption of duplicated loci. Research on polyploidy was highly biased towards plants during the last century because polyploidy in animals was for long time considered rare, occasional and irrelevant from an evolutionary perspective. However, as empirically observed in plants, genome rediploidization starts in polyploid organisms immediately after the polyploid shock. Given the speed and dynamicity of this process, evidence of genome multiplication is completely erased over time, and hence, only the most recent events are likely to be acknowledged. Although varying in expression between and within taxonomic groups, polyploidy and hybridization are ubiquitous in animals and may be recurrent, fostering evolution. Since evolutionary allopolyploid genomes behave as biologically diploid, zoologists have to challenge the old paradigm of an irrelevant evolutionary role in animals using current genomic and cytogenomic tools. These methods are most likely to reveal the role of polyploid mechanisms in producing evolutionary novelties. Nonsexual complexes are the perfect models to bridge the gap between empirical and theoretical research, while the evolutionary process is in action. Such animal complexes represent a transient stage that, in general, moves towards a polyploid stage, where bisexuality might be recovered, ultimately giving rise to a new gonochoric species. These pathways are herein illustrated by the Iberian allopolyploid Squalius alburnoides. Some general aspects on this fish's complex are updated and reviewed, namely the reproductive modes of the distinct genomotypes, since variable ploidies and genomic combinations occur in natural populations. Most recent data on the mechanisms of gene expression regulation and the importance of the genomic context in driving allelic expression are also included. It was first demonstrated that a regulatory mechanism involving dosage compensation by gene-copy silencing exists in allotriploid females and that allelic expression patterns differed either between genomically equivalent individuals or within the same individual (between tissues and genes). Thus, instead of a whole haplome inactivation, a biased silencing towards repression of a specific allele was observed as well as a reduction of the transcript levels to the diploid state. See also sister article focusing on plants by Tayalé and Parisod in this themed issue

Reproductive dynamics shapes genomotype composition in an allopolyploid complex

“…To control for size effects on fecundity, females were selected to show the least variation in length as possible, ranging between 5.7 and 7.2 cm. No similar size selection was possible for males, which generally differ in length among genomotypes [4], with PP males being the largest. Because spontaneous reproduction is hard to accomplish in captivity for isolated pairs of both S. alburnoides and S. pyrenaicus [19], outdoor tanks were compartmentalized for holding six mating pairs each.…”

“…Multiple mechanisms, such as mate choice, egg and sperm allocation, and offspring survival at early ontogenetic stages, may shape the dynamics of such hybrid populations to variable extents [4][5][6][7][8][9][10][11]. Clarifying those mechanisms is crucial to advance our knowledge regarding hybrids' ecology and evolution, namely, in allopolyploid vertebrates.…”

“…The vast majority of populations are dominated by allotriploids, namely, by the PAA genomotype in central and southern rivers. This highly female-biased genomotype is entirely maintained by crosses with other genomotypes (figure 1), because neither spontaneous parthenogenesis nor gynogenesis occurs in this complex and, thus, PAA females cannot restock their own genomotype without male genome incorporation (reviewed in [4]). This strict genomotype interdependency suggests that the structure of S. alburnoides populations may depend on an intricate reproductive dynamics, promoting the prevalence of the PAA genomotype, although empirical evidence to corroborate this is still mostly lacking.…”

Evolutionary history of two divergent Dmrt1 genes reveals two rounds of polyploidy origins in gibel carp

“…Recent polyploids have been identified in fishes and amphibians (Choleva and Janko, 2013;Gui and Zhou, 2010;Otto, 2007;Song et al, 2012) and some diploidized tetraploid species have been demonstrated in some teleost fish lineages including cyprinids, catostomids, and salmonids (Allendorf and Thorgaard, 1984;Collares-Pereira et al, 2013;Gui and Zhou, 2010;Yang and Gui, 2004), but the two recent rounds of polyploidy have been documented only in the polyploid gibel carp. Recent genome-wide studies have confirmed that the problem of genetic incompatibility raised by polyploidy may be resolved by the accumulation of diverse mutational changes to form a stable chimerical and diploidized genome (Buggs et al, 2011;Chen and Ni, 2006;Louis et al, 2012;Tate et al, 2009).…”

Gene copy silencing and DNA methylation in natural and artificially produced allopolyploid fish

“…It emerged between 1.4 million years ago (MYA) (Cunha et al, 2004) and less than 0.7 MYA (Sousa-Santos et al, 2007). In present days the complex comprises several ploidy levels and genomic compositions distributed across the Iberian Peninsula (Alves et al, 2001;Collares-Pereira et al, 2013). Taking advantage of the hybrid status of S. alburnoides, genome-specific sequence differences were used to determine the contribution of each parental genome to the overall expression of loci individually analyzed in diploid and triploid hybrid individuals (Pala et al, 2008).…”