Mate recognition and gamete cytology features allow hybrid species production and evolution in Bacillus stick insects

Abstract

The increasing number of recognized hybrid unisexual complexes among invertebrate and vertebrate animals has promoted investigations about their composition and origin. Morphological, karyological and genetic (protein and DNA) analyses clearly show that, owing to their persistence and incomplete reproductive isolation from ancestors, several all-female complexes are much more diversified than generally assumed and that they may also have an evolutionary role. Here the case of the stick-insects of the genus Bacillus is reported in some detail. This holomediterranean genus comprises three well differentiated species that in Sicily have hybridized repeatedly. THe Bacillus mate-recognition system has not follwed the species-specific differentiation of the allozyme-coding loci, allowing interspecidic crosses to occur in areas of species sympatry with the production of two hybridogens, a correponding allodiploid parthenogen and a trihybrid triploid parthenogenetic species. Hybridogenetic females eliminate the paternal haploset (grandii) while passing the unassorted rossius hemiclone to offspring, which will be agains of F1 hybrid structure through a real fertilization by host male sperm. The polyspermic eggs of the hybridogens can also produce full-paternal fertile progeny of both sexes (androgenetics), when mixis occurs between two sperm heads. The parthenogenetic mechanism of the corresponding hybrid B. whitei is very similar to the hybridogenetic one, excepting the automictic re-use of the sgregated grandii haploset; therefore, B. whitei offspring clonally maintain the maternal hybrid structure. The trihybrid B. lynceorum producees clonal descendants through an apomictic mechanism undergoind two seemingly normal meiotic divisions. Each Bacillus hybrid actually realizes a different egg maturation process; however, the three share one important feature: an intrameiotic DNA extra-doubling, leading to the formation of four-stranded chromosomes,. and enabiling the meiotic syste to produce balanced gametes even under different ploidy level and hybrid structure. The extra-round of DNA synthesis seems to be triggered by the hybrid condition impairing the synaptic process. Also the parthenogenetic B. whitei produces androgenetics and it is even capable of incorporating a third genome into its automictic but clonal eggs, following fertlization by B. grandii or B. rossius males with the production of fertlize triploids. These findings are evidence of clonal unisexual reproductively interacting with related bisexuals and also suggest that evolutionary pathways have been undertaken by Bacillus. Also other unisexual complexes seem to have undergone similar microevolutionary steps and their reproductive traits and persistence, longer than commonly assumed, make increasingly difficult to think of the whole of unisexuals as or