A mid-arm interchange as a potential reproductive isolating mechanism in the medically important Simulium neavei group (Diptera: Simuliidae)

Abstract

The Simulium neavei group is medically important as a vector of human onchocerciasis and is unique among blackflies because of the attachment to freshwater crabs during parts of the larval and pupal life cycle stages. Detailed larval salivary gland polytene chromosome maps are presented for two taxa designated S. neavei Amani form A and S. neavei Amani form B, which are probably synonymous with the previously described morphospecies, S. nyasalandicum and S. woodi, respectively. Simulium neavei Amani form B differs from S. neavei Amani form A by three paracentric inversions, a large deletion and a chromocentre, while the latter taxon differs from the former one by a mid-arm interchange. The fixed mid-arm interchange (1-tr) between two related taxa is unique among the Simuliidae. Detailed banding analysis of S. neavei Amani form B shows that, relative to S. neavei Amani form A, sections 16a, 16b, and 17c of the short arm of chromosome one (IS) have been inserted into section 69/70 of the short arm of chromosome three (IIIS). Assignment of directionality for this interchange inferred because of the near universality in the Simuliidae of a chromosome III long arm to short arm ratio of 2:1. We propose that the mid-arm interchange acted as a primary isolating mechanism because of the segregational load on F1 heterozygous interchange progeny. The magnitude of the segregational load would be dependent on the frequency of pairing and crossing-over between the transposed interstitial segment and its original counterpart in the chromosome complement. Nonpairing in the transposed region and normal random segregation would presumably lead to a 50% of gametes carrying the duplicated or deficient transposed segment, resulting in a segregation load of 50%. However, crossing-over in the paired interstitial region may greatly increase segregational load as result of multivalent formation at metaphase one (MI) and the generation of dicentric bridge(s) and acentric fragment(s) upon cell division. Such meiotic disjunction irregularities could lead to meiotic arrest, gametic loss and (or) cell restitution, and the eventual formation of polyploid (lethal) zygotes.

Heterochromatin and sibling species ofSimulium praelargums.l. (Diptera: Simuliidae)

“…Sibling IIIL-1.2 differs from IIIL-st by a two step fixed included inversion found on the long arm of chromosome III. Both siblings possess heterochromatinized IIIS polytene chromosome ends, while IIIL-1.2 is unique within the Simuliidae in that it exhibits a very large enhanced chromocentre that persists in normal somatic tissue (Rothfels 1979;Shields and Procunier 1982;Procunier 1984;Procunier and Muro 1994;Adler et al 2010), contrary to other chromocentre-containing taxa. In IIIL-1.2, the chromocentre occurs as a positively allocyclic heteropycnotic body in normal mitotic interphase cells of neuroblast ganglia, oogonia, and spermatogonia.…”

“…and Eusimulium, such events are thought to be precursors associated with speciation involving Robersonian fusions leading to new taxa; chromosome fusions resulting in karyotype number being reduced from 2n = 6 to 2n = 4 in Cnephia laponnica (Procunier 1982b). There is also evidence that such fixed transposition events involving large segments of DNA through a nonhomologous mid-arm interchange have also occurred, and they have been causally implicated with sibling speciation in the medically important Simulium neavei group in East Africa (Procunier and Muro 1994).…”

Chromosomal Translocations in Black Flies (Diptera: Simuliidae)—Facilitators of Adaptive Radiation?

“…Of the 15 or so independently derived translocations in the Simuliidae, 80% involve whole-arm interchanges (including the type described in this study). Additional translocation types include the transfer of an entire arm to the terminus of its sister arm [ 20 ], relocation of a portion of one arm to a nonhomologous arm [ 21 ], and transfer of two adjacent bands to another arm [ 22 ]. The dearth of fixed, intra-arm translocations might be related to the detrimental consequences for heterozygotes, such as meiotic disjunction problems [ 21 ].…”

“…Additional translocation types include the transfer of an entire arm to the terminus of its sister arm [ 20 ], relocation of a portion of one arm to a nonhomologous arm [ 21 ], and transfer of two adjacent bands to another arm [ 22 ]. The dearth of fixed, intra-arm translocations might be related to the detrimental consequences for heterozygotes, such as meiotic disjunction problems [ 21 ]. The ease with which one or a few translocated bands could be overlooked might, in part, explain their (apparent?)…”