The early evolutionary history of neo-sex chromosomes in Neotropical grasshoppers, Boliviacris noroestensis (Orthoptera: Acrididae: Melanoplinae)

Abstract

Abstract. Neo-sex chromosomes are an important component of chromosome variation in Orthoptera, particularly South American Melanoplinae species, which have proven to be outstanding experimental model system to study the mechanism of sex chromosome evolution in this group of insects. In terms of their origin, most derived sex chromosome mechanisms involve a Robertsonian fusion (i.e. translocation) between the ancestral X chromosome and an autosome. In the grasshopper, Boliviacris noroestensis Ronderos & Cigliano (1990) (Orthoptera: Acrididae: Melanoplinae), our results point to a small degree of differentiation (conserved homology between the XR arm and the neo-Y) of the neo-XY chromosomes, which may be of recent evolutionary origin. However, a simple centric fusion model does not explain their origin, mainly because of the observed reduction in the fundamental number (fN) of arms. We propose two models which, we hope, clarify the genesis of B. noroestensis neo-sex chromosomes. Records of karyotype variation in related species due to multiple rearrangements support our models. We propose a possible adaptive advantage for neo-sex chromosome carriers, such changes perhaps representing the primary force that increases their frequency within natural populations compared with non-fused translocated forms, and occurring without apparent detriment to the microevolutionary forces that may also act, at least at the beginning of the evolutionary history of individuals bearing such neo-sex chromosomes.

Uncovering the evolutionary history of neo-XY sex chromosomes in the grasshopper Ronderosia bergii (Orthoptera, Melanoplinae) through satellite DNA analysis

“…First the de novo origin of the neo-sex chromosomes involved an X-A centric fusion [ 27 , 28 ] that is the most accepted hypothesis for the neo-sex chromosome origin in Orthoptera [ 15 – 17 ]. After the neo-XY arisen, recombining events are still able to occur between the XR arm, which corresponds to the ancestral autosome involved in the rearrangement, and the neo-Y, as documented in other Melanoplinae species by chiasmata analysis [ 17 , 71 ]. After the neo-sex chromosomes have been established the C-shape disposition of neo-XY in meiotic metaphase led some authors to suggest the occurrence of a large pericentric inversion [ 15 , 16 ] involving more than 90% of the neo-Y followed by its heterochromatinization and recombination suppression between the neo-X and the neo-Y [ 15 , 16 , 20 ].…”

Neo-sex Chromosomes in the Maculipennis Species Group (Dichroplus: Acrididae, Melanoplinae): The Cases of D. maculipennis and D. vittigerum

“…However, R. bergii neo-Y shows a marked dispersion of this repetitive DNA fraction throughout the long arm of the neo-Y chromosome (Palacios-Gimenez et al, 2015). Research also suggests different accumulation/diversification patterns of repetitive DNAs of neo-Y chromosomes in this closely related species; such empirical data could be evidence for the loss of selection pressure in chromosomal regions in which recombination is abolished, leading to a high rate of genetic diversification (Palacios-Gimenez et al, 2013;Castillo et al, 2014;Palacios-Gimenez et al, 2015).…”

“…This impressive neo-sex chromosome diversity resulted from recurrent independent rearrangements starting from the standard X0/XX system in the evolutionary history of several lineages (Bidau and Martí, 2001;Mesa et al, 2001;Castillo et al, 2010b;Castillo et al, 2014). In general, when simultaneous centromeric breakage of the X chromosome and an autosome and subsequent fusion occur, a neo-sex chromosome arises (Castillo et al, 2010b) although other initial rearrangements may occasionally be involved (Bidau and Martí, 2001).…”

“…These properties vary continuously from the conservation of complete homology, full synapsis and chiasma formation in recently emerged systems, to almost complete degeneration and loss of homology of the neo-Y in putative ancient systems. Degeneration involves further chromosomal rearrangements, gene loss, and accumulation of non-coding repetitive sequences (Bidau and Martí, 2001;Mesa et al, 2001;Castillo et al, 2014;Palacios-Gimenez et al, 2013;Palacios-Gimenez et al, 2015). However, complete loss of the neo-Y, transforming the system into a "neo-X0/XX" one, has never occurred as far as the available information indicates .…”

“…However, complete loss of the neo-Y, transforming the system into a "neo-X0/XX" one, has never occurred as far as the available information indicates . Furthermore, there are several species exhibiting different structural and genetic instances of neo-sex chromosome systems in which a single A-X centric fusion does not explain their structure and complex meiotic behavior (e.g., Boliviacris noroestensis, Dichroplus vittatus) (Bidau and Martí, 2001;Castillo et al, 2014).…”