Rise and Persistence of Animal Polyploidy: Evolutionary Constraints and Potential

Abstract

The past decade has witnessed a tremendous increase in interest in polyploidy, which may partly be related to the development of new powerful genetic and genomic tools. These have provided numerous insights into mainly genetic and genomic consequences of polyploidy, dramatically improving our understanding of the dynamics of the polyploidization process and its importance as a mechanism in animal evolution. In contrast, several other aspects of polyploidization, such as physiology, ecology and development, have received considerably less attention. Our aim is not to make an exhaustive review of current knowledge about animal polyploidy, but rather to thoroughly elaborate on some very fundamental questions which still remain open or even neglected. In particular, we show that properties of new polyploid lineages largely depend upon the proximate way in which they arose, but the evolutionary pathways to polyploidy are often unresolved. To help researchers orientate amongst the number of pathways to polyploidy, we provide an extensive review of particular scenarios proposed in distinct animal taxa. We discuss how polyploidy relates to hybridization, particularly with respect to asexuality, and elaborate on whether clonal triploids may help to overcome the constraints of aneuploidy, thereby serving as a triploid bridge towards the establishment of new polyploid species. We further show that in most animal asexual complexes clonal lineages may become established only under one ploidy level (usually either di- or triploidy), and that it is rather rare to see the coexistence of successful clones of different ploidies. We discuss why the rate of polyploidization is higher in some taxa than in others, and what tools we have to evaluate the rate of polyploidization. Finally, we review some of the immediate physiological and developmental effects of polyploidy which are related to the genome size/cell size relation and show how studies of polyploidy may enhance the study of macroecology and developmental biology. See also the sister article focusing on plants by Weiss-Schneeweiss et al. in this themed issue.

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).…”

Genetic conflict, kin and the origins of novel genetic systems

“…At this point, there is little evidence that they are. Well-documented cases are limited to parasitic wasps and thrips, and there are many parthenogenetic lineages in which no intracellular bacteria have been detected [56,57]. There are some cases in groups other than parasitic wasps in which parthenogenetic lineages are Wolbachia or Cardinium infected while related sexual lineages are not [58,59].…”

Histological evidence that diploid hybrids of Cobitis taenia and C. elongatoides (Teleostei, Cobitidae) develop into fertile females and sterile males

“…This is due to environmental factors, mainly external fertilization and a weak ethological isolating mechanism (Stolzenberg et al, 2009). Fish of the family Cobitidae, especially the Cobitis taxa, are an interesting object to study hybridization and subsequent polyploidization processes (Saitoh et al, 2010;Choleva & Janko, 2013;Choleva et al, 2014).…”

“…The loaches of Cobitis in Central Europe occur mainly in mixed diploid-polyploid populations, in which individuals of spined loach C. taenia Linnaeus, 1758 and/or Danubian spined loach C. elongatoides Bacescu & Maier, 1969 co-exist with their diploid and polyploid hybrids (Boroń, 2003;Choleva & Janko, 2013;Choleva et al, 2014). Both of these species are small-sized, bottom dwelling fish.…”