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

A macrogenomic investigation of a Holarctic clade of black flies-the Simulium cholodkovskii lineage-provided a platform to explore the implications of a unique, synapomorphic whole-arm interchange in the evolution of black flies. Nearly 60 structural rearrangements were discovered in the polytene complement of the lineage, including 15 common to all 138 analyzed individuals, relative to the central sequence for the entire subgenus Simulium. Three species were represented, of which two Palearctic entities (Simulium cholodkovskii and S. decimatum) were sympatric; an absence of hybrids confirmed their reproductive isolation. A third (Nearctic) entity had nonhomologous sex chromosomes, relative to the other species, and is considered a separate species, for which the name Simulium nigricoxum is revalidated. A cytophylogeny is inferred and indicates that the two Palearctic taxa are sister species and these, in turn, are the sister group of the Nearctic species. The rise of the S. cholodkovskii lineage encompassed complex chromosomal and genomic restructuring phenomena associated with speciation in black flies, viz. expression of one and the same rearrangement as polymorphic, fixed, or sex linked in different species; taxon-specific differentiation of sex chromosomes; and reciprocal translocation of chromosome arms. The translocation is hypothesized to have occurred early in male spermatogonia, with the translocated chromosomal complement being transmitted to the X- and Y-bearing sperm during spermatogenesis, resulting in alternate disjunction of viable F1 translocation heterozygotes and the eventual formation of more viable and selectable F2 translocation homozygous progeny. Of 11 or 12 independently derived whole-arm interchanges known in the family Simuliidae, at least six are associated with subsequent speciation events, suggesting a facilitating role of translocations in adaptive radiations. The findings are discussed in the context of potential structural and functional interactions for future genomic research

Polytene chromosomes of an Indian Himalayan black fly Simulium (Nevermannia) praelargum (Diptera: Simuliidae)

High quality polytene chromosome maps (n=3) of a Himalayan Simuliid Simulium praelargum Datta, 1973 are presented and represent the first cytological description of a taxon found in the feuerborni group, subgenus Nevermannia. Polytene chromosomes one (I) and two (II) are metacentric, chromosome three (III) is submetacentric with the length of each chromosome occupying 37.25 %, 31.36 % and 31.34 % of the total complement length, respectively. Typical simuliid diagnostic intergeneric chromosomal markers are found within the polytene complement of this species. The nucleolar organizer (N.O.) is found at the base of the short arm of chromosome one (IS), the Ring of Balbiani (R.B.), double bubble (D.B.) and triad occur in the short arm of chromosome two (IIS), the Parabalbiani Ring (P.B.) and grey band (gb) occur in the long arm of chromosome two (IIL) and the Blister (BL) and Capsule (Ca) occur in the short arm of chromosome three (IIIS).Terminal bands at the end of IIIS are heterochromatinized and present atypically with respect to other simuliid fauna. Populations studied so far are unique among the Simuliidae in that they exhibit chromosome structural monomorphism. These high resolution polytene chromosome maps will form the basis for future cytological characterization and phylogenetic comparisons amongst members of the feuerborni group [Current Zoology 56 (4): 437–444, 2010]

IIS arm of <i>Simulium cholodkovskii</i> (female larva), showing the typical sequence (<i>IIS-1</i>,4,<i>5</i>,<i>6</i>).

<p>Limits of polymorphic inversions IIS-7–IIS-9 and IIS-11 are indicated by brackets; <i>6</i>_<i>a</i> and <i>6</i>_<i>b</i> denote alternative breakpoints for <i>IIS-6</i>. The standard sequence for the subgenus <i>Simulium</i> can be obtained from the <i>IIS-1</i>,4,<i>5</i>,<i>6</i> sequence by alphabetically ordering the fragments indicated by small letters ‘a’ through ‘n’ that appear below the chromosome. Ordering the fragments above the chromosome from ‘a’ to ‘h’ produces the Y-chromosome sequence (<i>IIS-1</i>,<i>5</i>,<i>6</i>,10) of <i>S</i>. <i>nigricoxum</i>, i.e. IIS-10 is Y linked (dotted lines), whereas IIS-4 is X-linked (dashed lines) and, therefore, absent on the Y. Bu = bulge, C = centromere, Hb = location of heteroband 43Hb, RoB = ring of Balbiani, tr = trapezoidal.</p

Frequency of rearranged constituents for all chromosomal rearrangements in the <i>Simulium cholodkovskii</i> lineage, relative to the <i>Simulium</i> subgeneric standard.

<p>Frequency of rearranged constituents for all chromosomal rearrangements in the <i>Simulium cholodkovskii</i> lineage, relative to the <i>Simulium</i> subgeneric standard.</p

Cytophylogeny of the <i>Simulium cholodkovskii</i> lineage, with terminals depicted by idiograms of each species.

<p>The outgroups (<i>S</i>. <i>erythrocephalum</i> and <i>S</i>. <i>vittatum</i>) are not shown on the cladogram. Rearrangements are shown in italics if fixed synapomorphies, in parentheses if polymorphic synapomorphies, and in square brackets if shared characters that could not be determined as plesiomorphic or synapomorphic. The homologues of each chromosome (I, II, III) are shown as tightly synapsed, and the arms are indicated as long (L) or short (S). Only diagnostic inversions (frequency > 0.10) for each species are shown on the idiograms. Fixed inversions are bracketed on the left. Polymorphic inversions are bracketed on the right as solid lines if autosomal, dashed if X-linked, and dotted if Y-linked. Landmarks are labeled on the idiogram for <i>S</i>. <i>cholodkovskii</i>: bl = blister with 2 heavy bands, Ce = centric region (with subscript indicating chromosome I, II, or III), em = end marker, Nk = neck, NO = nucleolar organizer, Pb = parabalbiani, RoB = ring of Balbiani.</p

IL arm of <i>Simulium nigricoxum</i> (female larva) from Canada, Thelon River, showing the <i>IL-1</i>,<i>17</i>,<i>18</i> sequence.

<p>The 3 fixed inversions are shown by a bracket (<i>IL-1</i>) and arrows (<i>IL-17</i>,<i>18</i>). The standard sequence for the subgenus <i>Simulium</i> can be obtained from the <i>IL-1</i>,<i>17</i>,<i>18</i> sequence by alphabetically ordering the fragments indicated by small letters ‘a’ through ‘l’. Limits of polymorphic inversions IL-19–IL-22 are indicated by brackets. C = centromere, Nk = neck.</p

IIIL arm of <i>Simulium decimatum</i>, showing continuity of transposed arms IS and IIIL and the <i>IIIL-2</i>,<i>15</i>,<i>23</i> sequence.

<p>The map represents a composite male (sections 98–100) and female larva, with sections 10–87 from the Thelon River and the remainder from the Tuul River. Polymorphic inversion IIIL-17, IIIL-19, and IIIL-25 (shared with <i>S</i>. <i>cholodkovskii</i>) are indicated by brackets. C = centromere, cs = cup and saucer marker, N.O. = nucleolar organizer.</p

IIL arm of the <i>Simulium cholodkovskii</i> lineage.

<p>A. <i>Simulium decimatum</i> (female larva), showing the <i>IIL-1</i>,<i>2</i>,18 sequence. <i>IIL-1</i>,<i>2</i> are not bracketed but the renumbered sections (56–60) in the base of the arm indicate their presence. B. <i>Simulium cholodkovskii</i> (composite female + male larva [proximal 5 sections]), showing the IIL-16 sequence. C. <i>Simulium cholodkovskii</i> (female larva), showing the IIL-17 sequence. C = centromere, DNA = DNA puff, gB = gray band, Hb = location of heteroband 69Hb, Pb = parabalbiani, pf = puffing band, ‘3’ = 3 sharp.</p

Collections of larvae of the <i>Simulium cholodkovskii</i> lineage used in chromosomal analyses.

<p>Collections of larvae of the <i>Simulium cholodkovskii</i> lineage used in chromosomal analyses.</p

Schematic derivation of the monocentric translocation homozygotes that define the <i>Simulium cholodkovskii</i> lineage.

<p>Diagnostic landmarks are given on idiograms for short (S) and long (L) arms of the three chromosomes (I, II, III). Both homologues of each chromosome are shown; bl = blister with 2 heavy bands, Ce = centric region containing putative centromere, em = end marker, Nk = neck, NO = nuclear organizer, Pb = parabalbiani, RoB = ring of Balbiani. Fixed inversions are italicized and bracketed on the left side of each chromosome; polymorphic inversions are in standard type and bracketed on the right side. A. Standard chromosomal complement, showing characteristic inversions of the <i>Simulium malyschevi</i> clade (<i>IL-1</i>, <i>IIL-1</i>, <i>IIL-2</i>, <i>IIIS-1</i>, and <i>IIIL-2</i>) from which the sequences of the <i>S</i>. <i>cholodkovskii</i> lineage are derived. From the ancestral intermediate through present-day members of the lineage (B–D), these inversions carry through as plesiomorphies, but are not shown in subsequent idiograms. B. Hypothetical intermediate of the <i>Simulium cholodkovskii</i> lineage, with characteristic fixed inversions established before the translocation event. Arrows 1 and 2 represent proximal and distal breaks, respectively, in the centric regions of chromosomes I and III. C. Derivation of a monocentric translocation heterozygote expressed as one of two possible scenarios: 1) As shown, chromosomal breaks occur in the proximal centric regions of chromosomes I and III (arrows 1 in Fig 10B) such that IS joins with CeIII plus IIIL and IL plus CeI joins with IIIS, giving rise to translocation heterozygote progeny (first generation). 2) (Not shown) chromosomal breaks occur in the distal centric regions of chromosomes I and III (arrows 2 in Fig 10B) such that IS plus CeI joins with IIIL and IL joins with CeIII plus IIIS. IIS is shown as the putative sex arm (X, Y). D. Monocentric translocation homozygote formed from an F1 mating. In our model, the first appearance of translocation homozygotes occurs in the F2 as a result of matings between F1 translocation males and females.</p