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Description of the karyotype of Sphyracephala detrahens (Diptera, Diopsidae)

Comparative Cytogenetics

December 2019
13(4):383-388

DOI:10.3897/CompCytogen.v13i4.47302

License
CC BY 4.0

Authors:

Ayumi Kudo

Yamaguchi University

The eye stalks in Diopsidae (Bilberg, 1820) have been widely examined, but the evolutionary origin of this unique trait remains unclear. Thus, further studies of Sphiracephala (Say, 1828), the extant genus forming a basal branch of Diopsinae, are needed. The present study aimed to identify the karyotype of Sphyracephala detrahens (Walker, 1860) with conventional Giemsa staining. Cytogenetic analysis revealed a diploid number of 2n = 10 including two pairs of metacentric chromosomes, a pair of telocentric chromosomes, a pair of dot-like chromosomes, and a pair of sex chromosomes in S. detrahens . The congener Sphyracephala brevicornis (Say, 1817) has been reported to have the same diploid number, 2n = 10, but different chromosome formula. These results demonstrate that chromosome rearrangements often occur in the genus Sphyracephala .

Stalk-eyed flies Sphyracephala detrahens.

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Mitotic metaphase of Sphyracephala detrahens with 2n = 10 chromosomes A female B male. Scale bars: 5µm.

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Idiograms of Sphyracephala detrahens and Sphyracephala brevicornis. The numbers above each bar indicate chromosome numbers. The light and dark regions represent short arms and long arms, respectively. Idiograms of S. brevicornis were modified and redrawn from Idiogram 1 of S. brevicornis (Jan 1966).

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Morphometric parameters of Sphyracephala detrahens chromosomes from mitotic metaphase plates.

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Sphyracephala detrahens karyotype 383

Description of the karyotype of

Sphyracephala detrahens (Diptera, Diopsidae)

Ayumi Kudo1

1 Department of Biological Sciences School of Science, Tokyo Metropolitan University, Minamiohsawa 1-1,

Hachiohji-shi, Tokyo 192-0397, Japan

Corresponding author: Ayumi Kudo (kudokudo1103@gmail.com)

Academic editor: I. Sharakhov|Received 14 October 2019|Accepted 31 October 2019|Published 3 December 2019

http://zoobank.org/022BF5FE-4994-474F-94D3-40AFFF0090AA

Citation: Kudo A (2019) Description of the karyotype of Sphyracephala detrahens (Diptera, Diopsidae). Comparative

Cytogenetics 13(4): 383–388. https://doi.org/10.3897/CompCytogen.v13i4.47302

Abstract

e eye stalks in Diopsidae (Bilberg, 1820) have been widely examined, but the evolutionary origin of

this unique trait remains unclear. us, further studies of Sphiracephala (Say, 1828), the extant genus

forming a basal branch of Diopsinae, are needed. e present study aimed to identify the karyotype of

Sphyracephala detrahens (Walker, 1860) with conventional Giemsa staining. Cytogenetic analysis revealed

a diploid number of 2n = 10 including two pairs of metacentric chromosomes, a pair of telocentric chro-

mosomes, a pair of dot-like chromosomes, and a pair of sex chromosomes in S. detrahens. e congener

Sphyracephala brevicornis(Say, 1817) has been reported to have the same diploid number, 2n = 10, but

dierent chromosome formula. ese results demonstrate that chromosome rearrangements often occur

in the genus Sphyracephala.

Keywords

Cytogenetics, chromosomes, karyology

Introduction

Nearly all species of Diopsidae (Bilberg, 1820) are well-known for their exaggerated

eye stalks (Shillito 1971). ere are approximately 160–8000 species and 10–15 gen-

era containing stalk-eyed ies in the family Diopsidae (Shillito 1971; Steyskal 1972;

Carr et al. 2006; Ovtshinnikova and Galinskaya 2016; Roskov et al. 2019). Although

CompCytogen 13(4): 383–388 (2019)

doi: 10.3897/CompCytogen.v13i4.47302

http://compcytogen.pensoft.net

Copyright Ayumi Kudo. 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.

SHORT COMMUNICATION

COMPARATIVE

Cytogenetics

International Journal of Plant & Animal Cytogenetics,

Karyosystematics, and Molecular Systematics

A peer-reviewed open-access journal

Ayumi Kudo / Comparative Cytogenetics 13(4): 383–388 (2019)

384

both males and females in Diopsinae have eyes that are laterally displaced from the

central head, the level of sexual dimorphism varies between and within species (Bur-

khardt and de la Motte 1985; Wilkinson and Dodson 1997; Meier and Hilger 2000).

Some species of stalk-eyed ies with extreme sexual dimorphism are used as model

organisms to study the evolution of sexually selected traits (Wilkinson et al. 1998; Carr

et al. 2005; Husak and Swallow 2011; Knell et al. 2013). For example, in Teleopsisdal-

manni (Wiedemann, 1830), morphology, sexual behavior, development, and cytology

has been widely studied (Wilkinson and Reillo 1994; Presgraves et al. 1997; Hurley

et al. 2002; Egge et al. 2011; Worthington et al. 2012; Cotton et al. 2015; Meade et

al. 2019). However, limited information regarding the ecology, biology, and cytology

of most stalk-eyed y species is available, particularly for monomorphic species and

primitive groups such as Sphyracepalini.

Sphyracephala shows the most likely ancestral state of extant Diopsinae (Kotrba

2004). Sphyracephala detrahens (Walker, 1860) is distributed in Taiwan, China, the Phil-

ippines, Indonesia, Papua New Guinea, and the southern islands of Japan (Ohara 1993).

A few studies have examined the ecology and morphology of Japanese populations, and

found the length of eye stalks less or not sexually dimorphic (Ohara 1993, 1997).

Although Baker and Wilkinson (2001) suggested that ancestral species in Diopsi-

nae share monomorphic eye stalks, Kotrba (2004) used cladistics analysis that includ-

ed the extinct species of Prosphyracephala to predict that sexual dimorphic eye stalks

evolved in early Diopsinae. To reveal the origin of eye stalks in Diopsinae, basic studies

including cytogenetic analysis of the species in Sphyracephalini need to be performed.

e current study aimed to describe the karyotype of S. detrahens using standard chro-

mosome staining.

Material and methods

S. detrahens was collected from Iriomote Island, Okinawa, Japan in April 2019 by A.

Kudo (Fig. 1).All ies were maintained on organic media with yeast at 25 °C in a 14-h

light:10-h dark cycle.

Metaphase chromosomes were obtained from cerebral ganglia of 3rd instar larvae

as described by Imai et al. (1988) without colchicine treatment. e chromosome

preparations were stained with 5% Giemsa solution. e preparations were observed

under a Keyence BZ-X700 uorescence microscope (Osaka, Japan) equipped with a

Nikon Plan Apo100×/1.45 oil objective and Nikon immersion Oil Type NF (Tokyo,

Japan). Twenty metaphase cells with well-spread chromosomes were selected and pho-

tographed using Keyence BZ-X Analyzer software, and then processed in GIMP ver. 2.

10. 12. Fifteen individuals including 10 females and 5 males were successfully karyo-

typed. e length of the long and short chromosome arm was measured with Image

J software ver. 1.52a (NIH, Bethesda, MD, USA). ese data were used to calculate

the chromosome index and arm ratio, following which chromosome classication and

idiogram construction were performed as described by Levan et al. (1964).

Sphyracephala detrahens karyotype 385

Figure 1. Stalk-eyed ies Sphyracephala detrahens.

Results and discussion

is is the rst study to reveal that the chromosome number of S. detrahens was 2n =10

(Fig. 2). e karyotype of S. detrahens consisted of two pairs of metacentric chromo-

somes, a pair of rod-shaped telocentric chromosomes, a pair of dot-like microchromo-

somes, and a pair of sex chromosomes (Figs 2, 3). In the female cerebral ganglia cells, a

homomorphic sex chromosome pair was formed by the two submetacentric X-chromo-

somes (Fig. 2A). In the male cerebral ganglia cells, a heteromorphic pair of sex chromo-

somes was formed by the X-chromosome and metacentric Y-chromosome (Fig. 2B). e

Y-chromosome was slightly stained and was shorter than the X-chromosome (Fig. 2).

Although a congener, S. brevicornis, had the same diploid chromosome number

2n = 10, the karyograms of S. brevicornis diered from that of S. detrahens (Fig. 3); the

karyotype of S. brevicornis consisted of two pairs of metacentric chromosomes, two

pairs of telocentric chromosomes, and a pair of small telocentric XY pair (Jan 1966).

Table 1. Morphometric parameters of Sphyracephala detrahens chromosomes from mitotic metaphase

plates.

Chromosome Length of short arm

(mean ± SE µm)

Length of long arm

(mean ± SE µm)

Total length of Chromosome

(mean ± SE µm)

Arm

ratio†

Centromeric

index‡

Chromosome

classication§

14.11 ± 0.15 4.45 ± 0.15 8.56 ± 0.29 1.08 48.0 m

22.49 ± 0.09 2.94 ± 0.10 5.43 ± 0.18 1.18 45.9 m

3– – 3.95 ± 0.14 – – t

4– – 0.66 ± 0.02 – – d

X1.63 ± 0.06 3.56 ± 0.11 5.19 ± 0.17 2.18 31.5 sm

Y1.80 ± 0.18 2.13 ± 0.24 3.93 ± 0.41 1.18 45.9 m

† Arm ratio = length of long arm/length of short arm;

‡ Centromeric index = length of short arm/total length of chromosome;

§ Chromosome classication; m: metacentric chromosome; sm: submetacentric chromosome; t: telocentric chromosome; d: dot-like

chromosome.

Ayumi Kudo / Comparative Cytogenetics 13(4): 383–388 (2019)

386

Figure 2. Mitotic metaphase of Sphyracephala detrahens with 2n = 10 chromosomes A female B male.

Scale bars: 5µm.

Figure 3. Idiograms of Sphyracephala detrahens and Sphyracephala brevicornis. e numbers above each

bar indicate chromosome numbers. e light and dark regions represent short arms and long arms, respec-

tively. Idiograms of S. brevicornis were modied and redrawn from Idiogram 1 of S. brevicornis (Jan 1966).

e sex chromosomes showed the greatest dierences between the two species. Both

the X and Y chromosomes in S.detrahens were bi-armed and larger compared to those

in S. brevicornis. us, chromosomal rearrangements occurred in these two species and

their relatives. Information about the phylogenetic relationships between S. detrahens

and its congeners has been never analyzed. Further investigations into phylogenetic

relationships will aid in the understanding of dierences in karyograms between S.

detrahens and S. brevicornis. Despite the lack of karyological information in Diopsinae,

comparative cytogenetic analyses using related species will lead to a greater under-

standing of chromosomal evolution in stalk-eyed ies.

Sphyracephala detrahens karyotype 387

Acknowledgements

I would like to thank Haruna Fujioka, Wataru Kojima and Yasukazu Okada for col-

lecting ies; Keiko Sakiyama for y maintenance; Kazuyuki Hirai for his technical

advice on chromosomal preparation; and Masafumi Nozawa for comments on karyo-

typing. I also thank Igor Sharakhov for comments on this manuscript.

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TRENDS ECOL EVOL

Many fossil animals bear traits such as crests or horns that probably functioned as sexually selected signals or weapons. Interpretations of these structures as functioning in mate choice or intrasexual contests are often controversial, with interpretations based on biomechanics or physiology being favoured by many. Although testing hypotheses based on sexual selection can be difficult, especially given that there is no single, reliable means of recognising sexual selection, we argue that it is not impossible; indeed, there are now several cases where sexual selection is strongly supported. In other cases, a careful study of features such as sexual dimorphism, ontogeny, and allometry, coupled with testing of alternative hypotheses, will be necessary to distinguish between possible explanations for exaggerated features.

Musculature of the male genitalia of a member of the genus Teleopsis Rondani, 1875 (Diopsidae, Diptera)

Article

Apr 2016

Secondary symmetry of pregenital sclerites and muscles, and also the presence of syntergosternite 7 + 8 and muscles between it and six segment in Diopsidae close this family to Psilidae and Nothybidae. Musculature of male genitalia in Teleopsis (Diopsidae, Diptera) is revealed and described for the first time. Morphology of hypandrium and its splitted muscles close this family to Nothybidae and advanced families of Cyclorrhapha, as Sciomyzidae, Scathophagidae and Calliphoridae.

Size matters, but so does shape: Quantifying complex shape changes in a sexually selected trait in stalk-eyed flies (Diptera: Diopsidae)

Article

May 2012

The elaborate morphologies of sexually selected ornaments are ubiquitous across the animal kingdom. In studies investigating these traits, ornament size is frequently the focus, and empirical evidence supports its positive correlation with fitness. Yet shape plays an important role and, surprisingly, is often overlooked. Shape frequently changes with size, influenced by biomechanical, developmental, or performance constraints. Therefore, shape can provide additional insights into the morphological differences between individuals and the potential limits on sexual trait exaggeration. Here, we used landmark-based geometric morphometric methods on a sexually dimor-phic species of stalk-eyed fly (Teleopsis dalmanni) to examine patterns of sexual shape dimorphism. Our analyses reveal a significant difference in head shape between the sexes, with males exhibiting smaller eye bulbs, thinner stalks, and smaller heads than females. Additionally, as eyestalk length increases within each sex, a similar pattern of shape change was observed as that observed between sexes. This pattern of shape change may be the result of constraints acting against further ornament exaggeration, and we suggest that this may significantly impact the whole-organism performance in stalk-eyed flies.

The genera of Diopsidae (Insecta: Diptera)

Article

Jun 2008
ZOOL J LINN SOC-LOND

JAMES F. SHILLITO

Taxonomic characters which have been used in defining the genera of Diopsidae are discussed with special reference to the structure of the head and eyestalks. In consequence, the subdivisions of this family put forward by Hennig in 1965 are revised and extended, a new scheme of three subfamilies being proposed and a possible phylogenetic sequence of genera suggested. A key for the identification of these subfamilies and current generic taxa is given.