Homoploid hybrid speciation and genome evolution via chromosome sorting

Abstract

Genomes of numerous diploid plant and animal species possess traces of interspecific crosses, and many researches consider them as support for homoploid hybrid speciation (HHS), a process by which a new reproductively isolated species arises through hybridization and combination of parts of the parental genomes, but without an increase in ploidy. However, convincing evidence for a creative role of hybridization in the origin of reproductive isolation between hybrid and parental forms is extremely limited. Here, through studying Agrodiaetus butterflies, we provide proof of a previously unknown mode of HHS based on the formation of post-zygotic reproductive isolation via hybridization of chromosomally divergent parental species and subsequent fixation of a novel combination of chromosome fusions/fissions in hybrid descendants. We show that meiotic segregation, operating in the hybrid lineage, resulted in the formation of a new diploid genome, drastically rearranged in terms of chromosome number. We also demonstrate that during the heterozygous stage of the hybrid species formation, recombination was limited between rearranged chromosomes of different parental origin, representing evidence that the reproductive isolation was a direct consequence of hybridization.

A new butterfly species from south Russia revealed through chromosomal and molecular analysis of the Polyommatus (Agrodiaetus) damonides complex (Lepidoptera, Lycaenidae)

“…The last published review of the subgenus includes 120 valid species (Eckweiler and Bozano 2016). Many of them have extremely local ‘dot-like’ distributions that are restricted to particular mountain valleys in the Balkan Peninsula, Asia Minor, Transcaucasus, Iran and Central Asia (Vila et al 2010, Lukhtanov et al 2015a,b, Eckweiler and Bozano 2016, Vishnevskaya et al 2016). This subgenus is a model system in studies of speciation (Lukhtanov et al 2005, Wiemers et al 2009), intraspecific differentiation (Dincă et al 2013, Przybyłowicz et al 2014), and rapid karyotype evolution (Lukhtanov and Dantchenko 2002a, Kandul et al 2007, Vershinina and Lukhtanov 2013, 2017).…”

“…The specific pubescence of costal area of forewings may be a useful morphological character to separate species in syntopy (Dantchenko and Churkin 2003), but it works only in certain cases. In spite of morphological similarity, the taxonomic and identification problems within the subgenus Agrodiaetus can be solved if chromosomal (de Lesse 1960a,b, Lukhtanov 1989) or molecular markers (Wiemers 2003, Kandul et al 2004, 2007, Lukhtanov et al 2005, Stradomsky and Fomina 2013), or their combination (Lukhtanov et al 2006, 2008, 2014, 2015a,b, Vila et al 2010, Lukhtanov and Tikhonov 2015, Shapoval and Lukhtanov 2015a, b) are applied. An unusual diversity of karyotypes is the most remarkable characteristic of Agrodiaetus .…”

Is homoploid hybrid speciation that rare? An empiricist’s view

“…Beyond this basic definition, complete agreement is lacking on key aspects of the process, such as the relative proportions of each parental genome present in a hybrid species, the mechanisms leading to reproductive isolation (RI), the degree of RI or the role played by hybridization in the process (Rieseberg, 1997;Abbott et al, 2010). While our understanding of HHS has been improved by detailed evolutionary case studies documented by recent reviews (Abbott et al, 2013;Yakimowski and Rieseberg, 2014;Payseur and Rieseberg, 2016) and empirical studies focused on mechanisms leading to HHS (Renaut et al, 2014;Selz et al, 2014;Lukhtanov et al, 2015), there is controversy concerning the criteria to identify and demonstrate HHS, and even the range of situations that HHS might encompass.…”

“…Furthermore, we think that if there is evidence that a hybridization event has given rise to an established, persistent, morphologically and ecologically distinct hybrid lineage, the recognition of this fact should not be compromised by whether or not we can demonstrate that hybridization was directly the cause of RI. Hybridization can be causative of mechanisms that contribute to enhancing RI in hybrid lineages, for example, the sorting of chromosomal rearrangements along the recombinational speciation model (Lai et al, 2005;Lukhtanov et al, 2015) or the occurrence of new traits that change mating patterns (Vereecken et al, 2010;Selz et al, 2014;Marques et al, 2016;Ma et al, 2016). In addition, intrinsic changes in the hybrids not directly causing RI between hybrid lineages and their progenitors may ultimately lead to external RI by facilitating the colonization of new niches (Grant, 1981;Gross and Rieseberg, 2005).…”

Evolution of genome size and genomic GC content in carnivorous holokinetics (Droseraceae)

“…In contrast to monocentric chromosomes, whose kinetochore formation is restricted to the small areas of the centromeres, holokinetic chromosomes lack primary constrictions and their kinetochores are formed along their poleward surfaces (Bure s et al, 2013;Cuacos et al, 2015). Holokinetic chromosomes, therefore, tolerate chromosomal fissions or fusions and do not allow more than two crossovers in meiosis (reviewed in Bure s et al, 2013;Heckmann and Houben, 2013) which may substantially affect genome and karyotype evolution of their bearers (Escudero et al, 2012;Bure s et al, 2013;Bure s and Zedek, 2014;Lukhtanov et al, 2015;S ıchov a et al, 2016). One such effect may be a negative correlation between genome size and chromosome number in holokinetic lineages (Nishikawa et al, 1984;Roalson et al, 2007; Z avesk a Dr abkov a and Vl cek, 2010;Bure s et al, 2013;Lipnerov a et al, 2013;Bure s and Zedek, 2014).…”