Research Article |
Corresponding author: Veronika V. Golygina ( nika@bionet.nsc.ru ) Academic editor: Igor Sharakhov
© 2018 Veronika V. Golygina, Iya I. Kiknadze.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Golygina VV, Kiknadze II (2018) The revision of chromosome III (EF) mapping in Chironomus plumosus (Linnaeus, 1758) group (Diptera, Chironomidae). Comparative Cytogenetics 12(2): 201-222. https://doi.org/10.3897/CompCytogen.v12i2.23327
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A revision of mapping of main and alternative banding sequences in chromosome III (EF) has been made for 14 species of the Chironomus plumosus group. In total, new versions of mapping are presented for 18 banding sequences of arm E and 18 banding sequences of arm F. A new way of tracing the origins of banding sequences in chromosome III of the Ch. plumosus group in comparison with basic banding sequences of the genus Chironomus is suggested. The presented data indicate that h’pluE2 in arm E and p’borF2 in arm F are the closest to banding sequences of Ch. piger Strenzke, 1959 and thus should be considered the most ancient among banding sequences of chromosome III in the Ch. plumosus group. Phylogenetic relationships of banding sequences of chromosome III are discussed.
Chironomus plumosus , Chironomus , Chironomidae , karyotype, polytene chromosome, banding sequence, chromosome III (EF), chromosome mapping, phylogeny, phylogenetic relationship, karyological analysis
The Chironomus plumosus group of sibling species presents a great opportunity for the study of the genomic reorganization at the chromosome level during speciation as most of the sibling species have wide geographic ranges with high levels of chromosomal polymorphism in natural populations (
Arm E is the most conservative arm in karyotypes of Ch. plumosus sibling species, as well as in the genus Chironomus (
However, h’pluE1 is also considered to be identical to banding sequences in arm E of many species from the genus Chironomus Meigen outside the Ch. plumosus group, such as Ch. aberratus Keyl, 1961, Ch. anthracinus Zetterstedt, 1860, Ch. cucini Webb, 1969, Ch. jonmartini Lindeberg, 1979 and several others (
Banding sequences of arm F also show a high level of conservatism among Chironomus species, although it is not as high as in arm E (
In this paper we present the results of revision of mapping for main (present in homozygotes in most populations with high frequencies) and alternative (present in homozygotes in some populations with high frequencies and in heterozygotes in most populations) banding sequences in chromosome III (EF) of 14 sibling species belonging to Ch. plumosus group.
Revision of chromosome III (EF) mapping was conducted for 14 Ch. plumosus sibling species: Chironomus agilis Shobanov & Djomin, 1988, Ch. prope agilis (working name “Ch. agilis 2”) (
Mapping of arms E and F was done according to Keyl-Devai mapping system (
Each banding sequence in each chromosomal arm is given a short designation as follows: three-letter abbreviation of the species name (for example, agi – for Ch. agilis, bal – for Ch. balatonicus etc.) is followed by the name of the arm and the serial number of banding sequence in this arm (according to the order of its discovery), and prefixed by a letter that indicates its geographical distribution – p’ for Palearctic sequences, n’ for Nearctic sequences, or h’ for Holarctic sequences (e.g. p’balE1, h’pluE2, n’entF4 etc.).
Equipment of the Centre of Microscopical analysis of biological objects SB RAS in the Institute of Cytology and Genetics (Novosibirsk) was used for this work: microscope “Axioskop” 2 Plus, CCD-camera AxioCam HRc, software package AxioVision 4 (Zeiss, Germany).
As was mentioned above, two versions of mapping of banding sequence h’pluE1 in comparison with standard banding sequence h’pigE1 are used in different publications.
The Keyl version suggests two inversion steps between h’pluE1 and h’pigE1 as follows (
This hypothetical banding sequence has never been found in any studied karyotypes of Chironomus species.
As h’pluE2 differs from h’pluE1 by simple inversion but initially was not directly compared to h’pigE1, its previous mapping was a derivative from h’pluE1 mapping (Table
However, our study of these three banding sequences leads us to believe that h’pluE2 is in fact closer to h’pigE1 and h’pluE1 originated from it, which required a slightly different position of inversion breakpoints:
Reasons for the suggested change in mapping of h’pluE1 and h’pluE2 are shown on Figure
Mapping comparison of banding sequences h’pigE1, h’pluE2 and h’agiA1 (identical to h’pluE1). a – comparison of h’pigE1 and h’pluE2, b – comparison of h’pigE1 and h’agiE1=h’pluE1. Centromeric bands are designated by arrows. Individual band in regions 3 and 4 of h’pigE1 are marked by small letters. Dotted lines connect identical discs in compared banding sequences. Red dotted lines indicate borders of regions, where banding patterns of compared banding sequences are identical.
Mapping of arm E main and alternative banding sequences in Ch. plumosus group before the revision.
Designation of banding sequence | Mapping of banding sequence |
---|---|
h’agiE1*† | =h’pluE1 KV‡: ( |
h’agi2E1* | =h’pluE1 KV: ( |
p’balE1* | =h’pluE1 KV: ( |
h’bonE1* | =h’pluE1 KV: (Kerkis et al. 1989, |
h’borE1* | =h’pluE1 KV: ( |
h’entE1* |
KV: 1a-2e 10g-10c 3f-4h 10b-5a 3e-a 11a-13g C ( GV: 1a-2e 10g-10c 3f-4b 3b-e 10b-4c 3a 11a-13g C ( |
h’entE2 | =h’pluE1 KV: ( GV: ( |
h’murE1* | =h’entE1¶ KV version 1: 1a-3e 4a-h 10b-5a 11d-10c 3f 12a-13g C (Ryser et al. 1983, KV version 2: 1a-2e 10g-10c 3f-4h 10b-5a 3e-a 11a-13g C ( |
h’nudE1* | =h’pluE1 KV: (Ryser et al. 1983, |
h’nudE2 | =h’murE1# KV: 1a-3e 4h-a 10b-5a 11d-10c 3f 12a-13g C ( |
h’pluE1* |
KV: 1a-3e 5a-10b 4h-3f 10c-13g C ( GV: 1a-3a 4c-10b 3e-b 4b-3f 10c-13g C ( |
h’pluE2 |
KV: 1a-3a 4d-h 10b-3b 4c-3f 10c-13g C ( GV: 1a-3e 10b-3f 10c-13g C ( |
h’sinE1* | =h’pluE1 KV: ( GV: ( |
h’spJE1* | =h’pluE1 KV: ( |
h’spKE1* | =h’pluE1 GV: ( |
h’suwE1* | =h’pluE1 KV: ( GV: ( |
p’useE1* |
KV: 1a-3e 5a 3f-4h 10b-5b 10c-13g C ( |
h’useE3 | =h’pluE1 KV: ( |
As all banding sequences in arm E of other species from Ch. plumosus group are either identical to or originated from the h’pluE1 it was required to make a revision of all of them.
Mapping of banding sequences according to the Keyl-Devai system for Ch. plumosus sibling species published up to now, is shown for both versions in Table
Phylogenetic relationship of main and alternative banding sequences in arms E and F before (a, c) and after (b, d) the revision. Main banding sequences are written in bold, alternative – in italic. Identical banding sequences enclosed in boxes, figures near the lines that connect banding sequences indicate numbers of inversion steps between them. Dotted lines enclosing some banding sequences inside a block indicate that mapping presented for these banding sequences differ from mappings of other banding sequences in the block, yet all banding sequences in the block were considered identical.
According to our analysis, the true phylogenetic relationships are shown on Figure
Mapping of banding sequences of Ch. plumosus sibling species in arm E after the revision. a h’agiE1.1 (identical to h’pluE1, h’ag2E1, h’bonE1, h’borE1, h’entE2, h’nudE1, h’sinE1, h’spJE1, h’spKE1, h’suwE1, h’useE3) b p’balE1.1 c h’murE1.1 (identical to h’entE1, h’nudE2) d h’pluE2.2 e p’useE1.1. Centromeric bands are designated by arrows.
It was believed previously that the main banding sequence of Ch. balatonicus is identical to h’pluE1. However, our analysis had shown that this species differs from all other species of Ch. plumosus group by the presence of complex pericentric inversion in chromosome EF (Figs
Banding sequences h’entE1, h’murE1, and h’nudE2 are identical and differ from h’pluE1 by one simple paracentric inversion. We believe that minor revision should be made for its breakpoints (Fig.
Banding sequence p’useE1 differs from h’pluE1 by simple inversion. Loginova and coauthors (Loginova et al. 1994) placed the left inversion breakpoint between bands 5a and 5b but closer analysis shows that the real breakpoint is situated between bands 5b and 5c as the latter – the wide fuzzy dark band – closely adjoins region 10c-g (Fig.
Mapping of arm E main and alternative banding sequences in Ch. plumosus group after the revision.
Designation of banding sequence | Mapping of banding sequence |
h’agiE1*† | =h’pluE1 |
h’agi2E1* | =h’pluE1 |
p’balE1* |
KV: 1a-3e 5a-10b 4h-3f 10c-13e C ‡ GV: 1a-3a 4c-10b 3e-b 4b-3f 10c-13e C§ |
h’bonE1* | =h’pluE1 |
h’borE1* | =h’pluE1 |
h’entE1* |
KV: KV: 1a-2e 11a-10c 3f-4h 10b-5a 3e-a 11b-13g C GV: 1a-2e 11a-10c 3f-4b 3b-e 10b-4c 3a 11b-13g C |
h’entE2 | =h’pluE1 |
h’murE1* | =h’entE1 |
h’nudE1* | =h’pluE1 |
h’nudE2 | =h’entE1 |
h’pluE1* |
KV: 1a-3e 5a-10b 4h-3f 10c-13g C GV: 1a-3a 4c-10b 3e-b 4b-3f 10c-13g C |
h’pluE2 |
KV: 1a-3a 4d-h 10b-3b 4c-3f 10c-13g C GV: 1a-3e 10b-3f 10c-13g C |
h’sinE1* | =h’pluE1 |
h’spJE1* | =h’pluE1 |
h’spKE1* | =h’pluE1 |
h’suwE1* | =h’pluE1 |
p’useE1* |
KV: 1a-3e 5ab 3f-4h 10b-5c 10c-13g C GV: 1a-3a 4c-5b 3f-4b 3b-e 10b-5c 10c-13g C |
h’useE3 | =h’pluE1 |
Banding patterns in arm F of Chironomus species are not as conservative as in arm E, but the arm is still considered to have a low level of polymorphism with many species sharing the same banding sequences and a lot of species that differ from each other by single inversion steps (
However, our analysis had clearly shown that the inversion that was previously defined as 11a-17d actually has different breakpoints, which in turn required re-evaluating relationships both between banding sequences inside the Ch. plumosus group and with the standard h’pigF1.
Mapping of arm F main and alternative banding sequences in Ch. plumosus group before the revision.
Designation of banding sequence | Mapping of banding sequence |
---|---|
p’agiF1*† | =p’pluF2 While all authors considered it to be identical to p’pluF2, the presented mapping of the banding sequence was different in different papers: 1a-d 6e-1e 7a-10d 18c-a 11a-17d 18d-23f C ( 1a-d 6e-1e 7a-10d 18e-a 11a-17d 19a-23f C ( |
p’agi2F1 | =p’agiF1 While authors stated that it is identical to p’agiF1, the presented mapping of the banding sequence was different in different papers: 1a-d 6e-1e 7a-10d 17d-a 11a-16g 18a-23f C ( 1a-d 6e-1e 7a-10d 18c-a 11a-17d 18d-23f C ( |
p’balF1 | =h’borF1 ( |
p’bonF1 | =h’pluF1 ( |
p’borF1 | 1a-10d 17d-11a 18a-23f C ( |
p’borF2 | no published mapping according to Keyl-Devai system |
h’entF1 | =h’pluF1 ( |
n’entF4 | 1a-d 6e-1e 19d-18a 11a-17d 10d-7a 20a-23f C ( |
h’murF1 | =h’pluF1 (Ryser et al. 1983, Kiknadze and Kerkis 1986, |
h’nudF1 | =h’pluF1 (Ryser et al. 1983, |
p’nudF2 | 1a-d 14a-15i 19d-18a 11a-13d 6e-1e 7a-10d 17d-16a 20a-23f C ( |
h’pluF1 | 1a-d 6e-1e 7a-10d 17d-11a 18a-23f C ( |
p’pluF2 | 1a-d 6e-1e 7a-10d 18c-a 11a-17d 18d-23f C ( 1a-d 6e-1e 7a-10b 18e-a 11a-17d 10dc 19a-23f C ( |
p’sinF1 | 1a-d 6e-5d 10d-7a 5c-1e 14f-17d 14e-11a 18a-23f C ( |
h’spJF1 | =h’pluF1 ( |
p’spKF1 | =p’suwF1 ( |
p’suwF1 | =p’borF2 1a-10b 18e-a 11a-17d 10dc 19a-23f C ( |
p’useF1 | 1a-d 6e-1e 7a-10d 18e-a 11a-17d 19a-23f C (Loginova and Beljanina 1994) |
Photos in Figure
Comparison of regions of inversion breakpoint between banding sequences p’borF1 and p’agiF1.
Aside from the general revision that affects all banding sequences in arm F of all species in the group, we have found that arm F of Ch. balatonicus required a major revision due to the presence of the pericentric inversion and several banding sequences of different species were in need of breakpoint correction.
Mapping comparison of banding sequences h’pigF1 and p’agiF1. Centromeric bands are designated by arrows. Individual band in the regions 10, 18 and 19 of h’pigF1 are marked by small letters. Dotted lines connect identical discs in compared banding sequences. Red dotted lines indicate borders of regions, where banding patterns of compared banding sequences are identical.
Mapping of banding sequences of Ch. plumosus sibling species in arm F after the revision. a p’agiF1.1 (identical to p’pluF2, p’ag2F1, p’useF1) b p’balF1.1 c p’borF1.1 d n’entF4.4 e h’murF1.1 (identical to h’pluF1, h’bonF1, h’entF1, h’nudF1, h’spJF1) f p’spKF1.1 (identical to p’borF2, p’suwF1) g p’nudF2.2 h p’sinF1.1. Centromeric bands are designated by arrows..
As was mentioned above, thorough analysis of the centromeric region of chromosome EF of Ch. balatonicus had shown that this arm had undergone complex pericentric inversion that differentiates it from the rest of Ch. plumosus group and thus p’balF1 is not identical to p’borF1 as was supposed previously. Mapping of this inversion proved to be very difficult due to the complexity of the rearrangement along with the fact that bands in the pericentromeric region are often weak, not well defined and can be very similar in appearance. The comparison of inversion region between p’balE1, p’balF1, h’nudE1 and h’nudF1 is shown on Figure
Main banding sequences h’entF1 and h’nudF1 are identical to h’pluF1 (Fig.
Main banding sequence p’sinF1 differ from h’pluF1 by 3 inversion steps and aside from corrections that follow from changes made to h’pluF1 require a minor revision of inversion breakpoints (Figs
As was observed in many previous studies, arm E remains the least polymorphic arm of the karyotype in the group. Out of 14 species 10 have identical main banding sequences with another 2 having the same banding sequence as alternative. Only one species – Ch. balatonicus – doesn’t share any banding sequences with other species due to the presence of pericentric inversion in the chromosome EF. This species is also the only one that differs from others by more than one inversion step in arm E.
Mapping of arm F main and alternative banding sequences in Ch. plumosus group after the revision.
Designation of banding sequence | Mapping of banding sequence |
---|---|
p’agiF1 | =p’pluF2 |
p’agi2F1 | =p’pluF2 |
p’balF1 | 1a-10b 18ed 17d-11a 18a-c 10dc 19a-21a 22d-21b [13gf] 22e-23f C |
p’bonF1 | =h’pluF1 |
p’borF1 | 1a-10b 18ed 17d-11a 18a-c 10dc 19a-23f C |
p’borF2 | 1a-10d 18c-a 11a-17d 18d-23f C |
h’entF1 | =h’pluF1 |
n’entF4 | 1a-d 6e-1e 7ab 19d-a 10cd 18c-a 11a-17d 18de 10b-7c 20a-23f C |
h’murF1 | =h’pluF1 |
h’nudF1 | =h’pluF1 |
p’nudF2 | 1a-d 6e-b 14h-17d 18c-a 11a-14g 6a-1e 7a-10b 18ed 10dc 19a-23f C |
h’pluF1 | 1a-d 6e-1e 7a-10b 18ed 17d-11a 18a-c 10dc 19a-23f C |
p’pluF2 | 1a-d 6e-1e 7a-10d 18c-a 11a-17d 18d-23f C |
p’sinF1 | 1a-d 6e-a 10b-7a 5b-1e 5cd 14g-17d 18de 14f-11a 18a-c 10dc 19a-23f C |
h’spJF1 | =h’entD1 |
p’spKF1 | =p’borF2 |
p’suwF1 | =p’borF2 |
p’useF1 | =p’pluF2 |
The revision in arm F has also mostly provided minor changes in the mapping of inversion breakpoints without affecting phylogenetic relationship of banding sequences inside the group. Aside of the placement of h’balF1 due to the presence of pericentric inversion the only significant change has come from the correction of inversion breakpoint of p’nudF2 which made it related to both h’nudF1 and p’pluF2. In general banding sequences in arm F show a moderate level of divergence comparable with what we observe in arm A, with three species that have species specific main banding sequences and only two species – Ch. balatonicus and Ch. sinicus – that don’t share any banding sequence with other species.
Considering the level of banding sequences divergence in both arms it can be stated that chromosome EF is the least divergent among the three big chromosomes of Chironomus.
At the same time the revision has shown the phylogenetic relationship of banding sequences of Ch. plumosus group sibling species and the rest of the genus are different from what was assumed previously as the closest to h’pigE1 and h’pigF1 are h’pluE2 and p’borF2. As both arm E and F are low polymorphic in the genus, many species share the same banding sequences. As was mentioned previously, h’pluE1 and p’borF1 were believed to be identical to banding sequences of many other species as their banding patterns are considered basic for the genus Chironomus (
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