Mate recognition and gamete cytology features allow hybrid species production and evolution inBacillusstick 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 followed the species-specific differentiation of the allozyme-coding loci, allowing interspecific crosses to occur in areas of species sympatry with the production of two hybridogens, a corresponding 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 again of F, 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 segregated grandii haploset; therefore B. whitei offspring clonally maintain the maternal hybrid structure. The trihybrid B. lynceorum produces clonal descendants through an apomictic mechanism undergoing 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 enabling the meiotic system 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 fertilization by B. grandii or B. rossius males with the production of fertile «synthetic» triploids. These findings are evidence of clonal unisexuals 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 «dead ends» or «blind alleys».

Genomic evolution in parental and hybrid taxa of the genusBacillus(Insecta Phasmatodea)

“…The finding verifies that androgenesis can occur in the field as previously hypothesized (Mantovani & Scali, 1992;Tinti & Scali, 1996). Androgenesis was evidenced in the Bacillus hybrid strains of B. rossius-grandii through a series of allozymic, chromosomal and cytological investigations (Mantovani & Scali, 1992;Tinti & Scali, 1993, 1995. These females, found in two isolated Sicilian areas (corners of north-western and south-eastern Sicily; Fig.…”

“…On the contrary, when these two species are compared to B. rossius a high degree of differentiation emerges. This is well supported by several diagnostic morphological characters, high Nei's distance values (Nei's D value = 1.23-1.62) and clear differences in karyotypes (Scali et al, 1995).…”

“…This conclusion is based on the observation that body and egg morphology, at light and scanning electron microscopy levels, although clearly diagnostic did not adequately substantiate the very high genetic divergence that electrophoretic results on 20 gene loci solidly supported. Roughly speaking, body morphology and ootaxonomy would indicate a similar degree of divergence among B. rossius, B. grandii, and B. atticus, whereas allozymes point to a 5-fold higher differentiation between B. rossius and B. grandii than between B. grandii and B. atticus (Scali et al, 1995).…”

“…The strictly bisexual B. grandii (2n = 34, XX female; 33, X0 male) is endemic to the Sicilian area and is differentiated into three formally described subspecies: B. grandii grandii located with a few relict populations in the Iblean region; B. grandii benazzii with demes scattered over a narrow coastal belt in northwestern Sicily and on the Island of Levanzo (Egadi Archipelago); B. grandii maretimi endemic to the Island of Marettimo (Egadi Archipelago). Also the all-female parthenogen B. atticus is differentiated into three races on the basis of allozyme and karyological characterization: the diploid B. atticus atticus (2n = 33-34) widely distributed in the central Mediterranean basin (Sardinia, Sicily, southern Italian peninsula, Croatia and Greece); B. atticus carius including the Greek and Turkish triploid demes (3n = 48-51) and a single diploid Turkish population (2n = 34); B. atticus cyprius (2n = 32) from the island of Cyprus (Scali et al, 1995).…”

New DAPI and fish findings on egg maturation processes in related hybridogenetic and parthenogenetic Bacillus hybrids (insecta, phasmatodea)

“…Actually, two bisexual species (B. rossius 2n 36 and B. grandii 2n 34), several facultatively parthenogenetic populations of B. rossius, three parthenogenetic thelythokous taxa (B. atticus 2n 34, B. whitei 2n 35, B. lynceorum 3n 52), and two different hybridogenetic strains (B. rossius-grandii grandii and B. rossius-grandii benazzii, 2n 35) have been reported within the genus (review by Scali et al, 1995). Since their ®rst description, the clonal B. whitei and the hemiclonal strains turned out to be the hybrids between B. rossius and B. grandii (Nascetti and Bullini, 1982;, with B. rossius as the maternal parent of both (Mantovani et al, 2001).…”