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An unusual case of gynandromorphism in Neurothemis tullia (Odo­ na­ta: Libellulidae)

Ashikur Rahman Shome, Mokhlesur Rahman & Mahabub Alam*

Department of Zoology, University of Dhaka, BD-Dhaka 1000, Bangladesh; mahabub.zoo@ du.ac.bd *Corresponding author

Abstract. An unusual gynandromorphic individual of Neurothemis tullia is reported from Faridpur District in Bangladesh. The head and thorax, including wings, are clearly bilater- ally gynandromorphic. The abdomen is entirely pruinose androchromic with very few light spots left, however the abdominal tip bears female appendages. This unusual combination of gynandromorphism and androchromy is discussed in respect of its possible origin. Further key words. Dragonfly, Anisoptera, androchromy

Introduction Gynandromorphs are genetically and phenotypically chimeric specimens bearing separate male and female somatic characters in the same individual (e.g., Narita et al. 2010; Rosa & Zettel 2018). In contrast, intersexes are genetically uniform organisms. (e.g., Laugé 1985). Gynandromorphism is a rare phenomenon and usu- ally detected only among the strong sexually dimorphic species. It has been dem- onstrated in different arthropod taxa such as Crustacea Farmer( 2004), Arachnida, e.g., scorpions (Cokendolpher & Sissom 1988), spiders (Palmgren 1979), ticks (Labruna et al. 2002), and Insecta, e.g., stoneflies Klotzek( 1971), hymenopterans (Donisthorpe 1929; Pereira et al. 1994; Gjershaug et al. 2016), beetles (Le Gall 2006), butterflies Nielsen( 2010) and dipterans such as mosquitoes (Kronefeld et al. 2013) and fruit flies Morgan( & Bridges 1919; Patterson & Stone 1938). Gyn­ andromorph individuals have even been found in vertebrates such as reptiles (Kroh­ mer 1989), birds (Agate et al. 2003) and mammals (Gowen & Stadler 1956). In dragonflies, gynandromorphism is extremely rare Corbet( 1962). It has been recorded in seven odonate families, mostly Anisoptera (Ris 1929; Schiemenz 1953; Gloyd 1971, 1975; Belle 1976; Siva-Jothy 1987; May 1988; Ishizawa 1990; Sugi­mura et al. 2001; Tennessen 2008; Torralba-Burrial & Ocharan 2009; Pix 2011). Gynandromorphism is expected to be especially conspicuous in odonates with strong sexual colour dimorphism such as Neurothemis tullia (Drury, 1773). In this libellulid males and females differ strongly in wing colour and pattern Seehausen( 2017). It is a common and widespread species in tropical and subtropical main- land Asia and is usually abundant at swamps, weedy marshes, edges of wetlands, paddy fields and heavily-weeded tanks (Nair 2011; Andrew 2013). In Bangladesh,

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N. tullia is widely distributed and it flies throughout the year (Habib et al. 2016). It typically perches on twigs, aquatic weeds along the border of water bodies not more than five feet above ground. Here we present an unusual case of an incomplete bilateral gynandromorph combined with extraordinary morphological characters on the abdomen.

Material and methods Data on Neurothemis tullia were obtained on 29-viii-2017 at a small overgrown pond in Faridpur district (23°36’25.83’’N, 89°50’18.83’’E), Bangladesh. Other Odo- nata species found were Brachythemis contaminata, Crocothemis servilia, Diplacodes trivia­lis, Ictinogomphus rapax, N. fulvia, Orthetrum sabina and Rhodothemis rufa. Dra­gonflies were abundant at the time. Odonates were observed with the naked eye and photographed using a Nikon D7100 DSLR Camera with an 18–140 mm VR lens.

Results While observing dragonflies at the pond we noted an aberrant individual ofNeuro­ themis tullia flying at the edge of the water. When it perched we were able to pho- tograph it (Fig. 1). However, our attempts to collect the aberrant individual failed. Therefore, the morphological characteristics of this individual were analysed on the basis of photographs only (Table 1). The head and thoracic coloration including the wings were clearly male on the right side and female on the left. On the other hand, the abdomen is entirely dark and pruinose with only few small light spots left as occurs in old males, whereas the abdominal tip bears two short, well separated cerci, typical of females.

Discussion The individual of Neurothemis tullia observed by us exhibits a mosaic combination of male and female external characters (cf. Fig. 1). The head and thorax are clearly bilaterally gynandromorphic whereas the coloration of the abdomen is male-like. On the other hand, the abdominal tip with the appendages (cerci) is female. The whole abdomen may either be female with male pruinosity or it could be genetically male and at the tip female, thus exhibiting anterior-posterior mosaic gynandromor- phism. It seems likely that the abdomen is mostly genetically male as pruinosity has never been reported in old females of N. tullia (R. Dow, M. Seehausen pers. comm.). Gynandromorphism is a very rare phenomenon in Odonata and to date only about 30 such individuals have been documented (Tennessen 2008; Torralba-Burrial & Ocharan 2009). It is a complex multifactorial issue caused by different genetic and environmental factors. From the genetic perspective, the female sex in Odonata is generally determined by XX and male sex is determined by XO (Shrivastava & Das 1953; Omura 1955; Kiauta 1969). Mitotic defects during embryonic de- velopment may result in gynandromorphs. At an early stage of a female embryo, a

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Table 1: Neurothemis tulia – morphological characteristics of the gynandromophic indi- vidual compared to those of both genders, based on photographs and descriptions by See- hausen (2017).

Male Female Gynandromorph Frons Very dark brown to metallic Dark brown Dark metallic blue blue Eyes Upper part brown to very dark Upper part brown, Left eye as in purplish-brown, lower part lower part green- female, right eye green-brown brown as in male Wings Young males brown with red- Basal half tinted yel- Left wings as in dish veins on basal half beyond low with dark brown female with white nodus, then deep black with spot around nodus and band faint, marginal opaque white band brown subcostal area, right wings as in which may be absent, apices with or without white male transparent band, apices dark brown Thorax Dark brown to almost black Yellowish green with Left side as in (pruinose when mature), dor- dark brown stripe on female, right side sally broad yellowish-green each side as in male stripe Abdomen Young males black on sides, Bright yellowish- green Both sides dark dorsally with bright yellowish- with dark brown stripe blue, heavily devel- green longitudinal stripe devel- on either side oped pruinosity as oping dark bluish pruinosity in in old males, with aging males, only some or no few small bright bright markings remaining spots remaining S10 and Cerci (superior appendages) Cerci about half as long Cerci as in female: appendices about as long as S10 or longer, as S10 or slightly long- slightly longer than slightly curved and close to- er, well separated from half as S10, well gether, inferior appendage each other, inferior separated from present appendage absent each other, appen- dix inferior absent single cell may lose one X chromosome and the tissue resulting from it has the male chromosome constitution (XO). If this mistake happens in the first cell division of the zygote the consequence will be an asymmetric individual, male on one side and female on the other (bilateral gynandromorph) as first demonstrated in Drosophila melanogaster (Morgan & Bridges 1919). If this happens later, an individual will exhibit a mosaic pattern having male and female patches across the body (mosaic gynandromorph) as, e.g., manifested in Calopteryx virgo (Ris 1929). Because the genetic constitution of the gynandromorph individual of N. tullia presented here is not known, the mechanism of its formation must remain obscure. The situation is complicated by the fact that in N. tullia sex determination may be partially by XX–XY (Chaudhuri & Gupta 1949), the latter probably corresponding to the neo-

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XY-type (Kiauta 1969). Apart from this, partially delayed fertilization, dispermy in eggs with two nuclei, early egg development, heritable cytoplasmic effects may also be responsible for gynandromorphism (Gordh & Headrick 2001). To our knowledge, this is the first report on gynandromorphism in N. tullia, al- though there are accounts of andromorphic females (Kumar 1988; Mitra 1991; Prasad et al. 2000; Andrew 2013). An alleged gynandromorphic specimen re- ported from Kerala, India (Emiliyamma 2009), could not be confirmed. According to the description it was most likely an andromorph female, not a gynandromorph. In insects, gynandromorphic specimens have been documented from 69 fami- lies in 13 orders (Cui & Cui 2003). In Odonata, gynandromorphism is reported from seven families so far: Calopterygidae, Coenagrionidae, Aeshnidae, Gomphi- dae, Cordulegastridae, Corduliidae, and Libellulidae (Tennessen 2008; Pix 2011). Most of the known gynandromorphic individuals are Anisoptera. Bilateral gyn­ andromorphism was recorded from several species in different parts of the world in- cluding Argentina (Belle 1976), France (Siva-Jothy 1987), Germany (Schiemenz 1953; Pix 2011), Japan (Gloyd 1971; Ishizawa 1990; Futahashi et al. 2019), Spain (Torralba-Burrial & Ocharan 2009) and USA (May 1988; Tennessen 2008).

Fig. 1 Gynandromorph individual of Neurothemis tullia. Faridpur district, Bangladesh (29- -viii-2017). Photo: ARS

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Acknowledgements. The authors are grateful to Hansruedi Wildermuth for his critical com- ments and suggestions to improve the manuscript.

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