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Gynandromorphism is a rare phenomenon where an individual develops with a mosaic of both male and female traits. It is observed in various groups of organisms, including arthropods, birds, reptiles, amphibians, and mammals. Among arthropods, gynandromorphs have been frequently documented in both natural populations and laboratory settings. In insects, bilateral gynandromorphs are the most commonly observed, where the left and right halves of the body display different sexes. This phenomenon has been reported in 12 orders within the class Insecta. Within the order Lepidoptera (butterflies and moths), gynandromorphism has been documented in 18 families, with a higher number of cases observed in the families Papilionidae, Pieridae, and Saturniidae. Lepidopterans are known for their sexual dichromatism, primarily expressed through wing coloration. While gynandromorph specimens have been reported in various butterfly families such as Lycaenidae, Nymphalidae, Pieridae, Papilionidae, and Geometridae, there have also been documented cases in certain moth species, including Noctuidae species like Agrotis segetum and Agrotis ipsilon.
Department of Agricultural Entomology, Visva-Bharati University, West Bengal, India
Satya Narayan Satapathy*
Faculty of Agricultural Sciences, Department of Entomology, Siksha ‘O’ Anusandhan Deemed to be University, Bhubaneswar, Odisha, India
*Address all correspondence to: satyanarayansatapathy40@gmail.com
1. Introduction
Gynandromorphism is a condition where a single individual develops with a combination of male and female characteristics [1]. A gynandromorph is a chimaera individual whose body has both masculine and feminine parts [2]. The term ‘gynandromorph’ is derived from the Greek words (gyne = woman; aner = man and morphe = form). It is extremely uncommon in arthropods, as compared to plants. To put in another way, arthropods are sexually dimorphic, which means that each individual develops into either an entirely male or an entirely female but does not become an intermediate. Yet several gynandromorphs, particularly in arthropods, have been reported both in natural and laboratory populations. These morphologically abnormal individuals who possess mixed male and female characteristics might result from developmental defects which are rare in natural environments. Gynandromorphs have been estimated to occur in insect populations at a frequency of 0.01 to 0.05% of their natural occurrence [3]. Along with arthropods, this peculiar phenomenon has been described in birds [4], reptiles [5], amphibians [6], fish [7] and mammals [8]. Gynandromorphs are often exhibited in two ways: bilaterally and non-bilaterally (sexual mosaics), depending on how male and female characteristics are distributed throughout the body. Additionally, they can be categorized as anteroposterior (where the anterior and posterior sides are of different sexes), bilateral (where the right and left sides are of different sexes), transversal (where the distribution is asymmetric), or mosaic (where the features are distributed randomly over the body). Embryogenesis defects at early phase leads to the formation of insect’s body part that are marked with characters of different sex. The aberrant division of nuclear substance during the division of the fertilized egg is the cause of gynandromorphism. If this occurs at the very first division, a bilateral gynandromorphism develops. The gynandromorph will be a mosaic if such an abnormality happens in the later phases of the egg division. In insects, the bilateral form most commonly occurs when the left and right portions are of different sexes. In contrast, mosaics have both sexual features mixed together and unevenly dispersed throughout the body, giving it a patchy appearance [9].
Numerous studies have documented the existence of arthropods with phenotypically male and female parts. These individuals exhibit a various of male and female part distribution patterns. For instance, the male and female reproductive organs may be distinctly bilateral, unevenly distributed, or mixed. Although this classification is frequently used, it does not take into account the genetic and developmental processes. Twelve orders of the class Insecta have bilateral gynandromorphs. Gynandromorphism is a well-known phenomenon among Lepidoptera, but it can occur more or less frequently depending on the group. In Lepidoptera, presence of gynandromorphism is at low rate (0.000125%), that is, one in 8000 reared insects. Lepidopteran gynandromorphs have been found in species that exhibit sexual dimorphism, indicating different morphological characteristics of male and female, such as wing pattern and antennae. Because of this, two halves of the adult insect exhibit distinct sexual phenotypic characteristics. There have been reports of gonandromorphism from 18families in this order. Among them, a lot of specimens have been reported for butterfly species (e.g., in Geometridae, Lycaenidae, Nymphalidae, Pieridae, Papilionidae) [3, 10, 11, 12, 13, 14, 15] and also for moths (e.g., Noctuidae) [16, 17]. However, the Papilionidae, Pieridae, and Saturniidae families account for the majority of cases [9].
Boveri’s hypothesis. A postponement in the fusion of the spermatozoon with the egg, causing the egg to initiate cell division before the sperm nucleus reaches it, resulting in only half of the egg being fertilized.
Only one polar body is extruded; In Hymenoptera, a second maturation division occurs after which two ootids are formed. Of these two ootids, one undergoes fertilization and develops into female parts, while the other ootid remains unfertilized and develops into male parts.
Morgan’s first hypothesis. In certain cases, multiple spermatozoa enter the egg, resulting in a unique reproductive process. One of the spermatozoa successfully fertilizes the egg, giving rise to the development of female parts. Meanwhile, the development of male parts occurs through the utilization of one or more of the remaining spermatozoa. This mechanism allows for the formation of both female and male structures.
Morgan’s second hypothesis. At the first division of the fertilized egg or during subsequent cell divisions, an X-chromosome is eliminated. This process results in the loss or exclusion of one of the X-chromosomes from the developing cells.
Through a process called non-disjunction, an individual with three X-chromosomes (XXX) can be produced. When the fertilized egg divides for the first time or after subsequent cell divisions, one of the X-chromosomes separates and moves to a cell, while the other two X-chromosomes pass to the other cell. In Lepidoptera, the cell that contains two X-chromosomes would give rise to male parts, while the cell with only one X-chromosome would develop into female parts.
In certain cases, such as in Abraxas, a binucleate ovum can occur where each different nucleus is fertilized by a different spermatozoon. Both nuclei in this binucleate structure may originate from the egg itself. However, in species like Bombyx mori (silkworm), one nucleus may be an egg nucleus while the other is a polar nucleus. The polar nucleus is typically involved in the process of polar body formation during oogenesis.
The pupa experiences mechanical shock as it sheds its larval skin.
In Lepidoptera, it is believed that most gynandromorphs (organisms with both male and female characteristics) likely originate from binucleate eggs of different types. The elimination of an X-chromosome has been demonstrated to cause gynandromorphism in Abraxas, but it can only be confirmed when a sex-linked trait is involved, and very few such traits are known in Lepidoptera. There is one known example of a mosaic pattern developing as suggested in the initial hypothesis by Hlorgan, indicating that some gynandromorphs may be produced in this manner. Somatic non-disjunction is considered the most probable explanation for Lepidopterous gynandromorphs, where only a small portion of the organism is male. In these cases, the individuals would begin as females (XY), and the male parts would possess an additional X chromosome (XXY). However, further confirmation is needed regarding the production of gynandromorphs through shock or other external factors (Figure 1).
Figure 1.
Sex determination in lepidopteran insects. (This model operates under the assumption that the functioning of a key/master regulatory gene, analogous to sex-lethal in insects, is influenced by the combined actions of maternal genes and zygotic genes. The regulatory gene’s expression plays a pivotal role in either activating or inhibiting the expression of subsequent genes (referred to as downstream genes). Progressing through the hierarchical cascade of gene expression, a highly conserved gene similar to double sex undergoes alternative RNA splicing, resulting in the production of either the male-specific DSX M protein or the female-specific DSX F protein. These sex-specific DSX proteins then go on to activate or suppress a set of genes responsible for sex-specific differentiation, ultimately leading to the development of either the male phenotype or the female phenotype.
In arthropods, the existence of individuals with phenotypically male and female parts has frequently been documented. They have been discovered in populations of all orders of non-insects as well as in insects both in natural environments and in laboratory populations. The term “gynandrous” or “gynandromorphous” was used to describe them long before any dissections were performed. Rudolphi performed the first dissection on a half-gynandromorphous Gastropaha quercifolia, the lappet (Lepidoptera: Lasiocampidae), in 1825 [18].
Conventional karyotyping is commonly practised for determining the sex of species where molecular analyses are not feasible. Simply observing the sex chromatin in lepidopteran insects with a ZW-ZZ sex chromosome constitution enables us to distinguish between the male (ZZ) and female (ZW) genotypes. The sex chromatin refers to a tightly compacted W chromosome that can be observed within interphase nuclei [19]. For insects where molecular data is accessible, distinguishing between male and female genotypes can be achieved through diagnostic polymerase chain reaction (PCR) amplifications using Y-specific or W-specific molecular markers. This technique enables the identification of genetic markers unique to the Y chromosome in males or the W chromosome in females. Furthermore, analyzing the transcriptional activity of genes that are expressed in a sex-specific manner can serve as an additional method to confirm the male and female phenotypes within an individual.
Gynandromorphs, which consist of individuals with a combination of male and female anatomical features, can occur naturally or be induced experimentally in various animal species. These individuals typically exhibit a mosaic appearance, where male and female tissues coexist, often following a symmetrical pattern. Bilateral gynandromorphs possess male characteristics on one side of the body and female characteristics on the other side. Transverse gynandromorphs, also known as polar gynandromorphs, exhibit a clear division between male and female body parts along a transverse plane perpendicular to the main body axis. The third type, oblique gynandromorphs, display a diagonal boundary between the different-sex body parts, crossing the sagittal plane at an angle [20]. Gynandromorphism has been observed in various species, primarily insects, chelicerates (spiders and mites), crustaceans, and birds. In contrast to gynandromorphism, which can be classified based on symmetry, the patterns of phenotypic expression in intersexual states are more specific to each taxonomic group.
Patterns of intersexuality encompass the characterization of sexually dimorphic anatomical structures and body organs, such as genitalia and gonads, that are affected by the anomaly. In the case of Armadillidium vulgare, a type of isopod, Legrand, Juchault [21] have identified four primary intersex types: (1) functional males displaying female genital openings; (2) individuals possessing a functional ovary accompanied by a vestigial testicular vesicle and underdeveloped vas deferens; (3) female individuals closely resembling the previous category, distinguishable primarily through physiological differences; and (4) males with testes that possess an oviduct.
Gynandromorphism is exceedingly uncommon in the natural world. Due to its rarity, the collection and description of gynandromorph specimens have been infrequent (0.01 to 0.05%).
A large number of gynandromorphs have been reported in Lepidoptera from at least 10 different species of Papilionidae, eight species of Lycaenidae, four Hesperiidae, ten Pieridae, four Nymphalidae, and several families of moths including Saturniidae, Pyralidae, Geometridae, and Lymantriidae (Table 1) [22, 23, 24, 25, 26].
In a study by Seven, Özdemir [3], a gynandromorphic specimen of Gnopharmia cholcidaria (Lederer, 1870) was documented, displaying lateral deviations. The left side of the specimen exhibited female characteristics, while the right side displayed male traits. Notably, the gynandromorphic individual of G. cholcidaria demonstrated distinct differences between the two sides.
On one side, the antenna was bipectinate, the wings were smaller in size, and the frenulum consisted of a single hair. Conversely, on the other side, the antenna appeared filiform, the wings were larger, and the frenulum exhibited a hair bundle shape. This dichotomy in antenna structure, wing size, and frenulum characteristics clearly distinguished the male and female traits within the gynandromorphic specimen of G. cholcidaria. Another gynandromorphic individual of Idaea deversaria (Herrich-Schäffer, 1847) exhibited frontal deviations. In this case, both sides of the specimen had filiform antennae, similar wing measurements, and a frenulum with a hair bundle shape resembling the female characteristics. Additionally, the hind legs lacked hair and shared the same shape on both sides. While the male genitalia structures dominated in G. cholcidaria, the characteristics related to male and female genitalia were found to be equal in I. deversaria. This indicates that the expression of genitalia traits in the gynandromorphic specimens varied between the two species.
Jahner et al. [13] studied comparing the genitalia and wing patterns of gynandromorphic Melissa blue butterflies (Lycaeides melissa) and one gynandromorphic Anna blue butterfly (L. anna) with the morphology of normal individuals, both from wild-caught specimens and those reared from wild populations. The researchers aimed to investigate the underlying mechanisms of gynandromorphism in Lycaeides species. It is commonly expected that Lycaeides bilateral gynandromorphs arise from double fertilization of a binucleate egg, which is considered the most prevalent mechanism of gynandromorphism [18, 27]. However, in certain cases, mosaicism can also occur in Lepidoptera due to the loss of the W chromosome during a nondisjunction event that takes place in later stages of development.
In Lepidoptera, the W chromosomes generally carry limited genetic information, and sex determination is primarily based on the number of Z chromosomes present in a cell. Males possess two copies of the Z chromosome, while females have only one [28]. This information suggests that the sex of an individual is predominantly determined by the number of Z chromosomes rather than the presence of W chromosomes.
In 2010, Rajkhowa et al. [29] reported a rare occurrence of bilateral gynandromorphy in the muga silkworm, Antheraea assamensis Helfer, discovered in Lahdoigarh, Assam, India. This unique gynandromorph specimen exhibited male characteristics on the left wings and female characteristics on the right wings. Notably, the wings on one side of the body were larger and darker compared to the other side. The measurements revealed a wing expanse of 75 mm on the left side (male) and 80 mm on the right side (female).
Distinct differences were observed in the antennae of the gynandromorph. The male antenna displayed a dark brown color with reddish-pink bases, while the female antenna appeared paler. The abdomen of the specimen was chestnut brown in color. The wing lines on the left side (male) were somewhat whitish, incurved, and outlined by dark brown, whereas on the right side (female), the wing lines were dark brown, incurved, and outlined by white. The left wings of the gynandromorph were dark brown, resembling the male, while the right wings were light pale brown, resembling the female.
In A. assamensis Helfer, both male and female individuals possess antennae that are quadripectinate, meaning they have four branches. Interestingly, the gynandromorph specimen exhibited pectens of different sizes, which are characteristic features of both males and females. This complete bilateral gynandromorphy is evident from the morphological variations observed.
Sagar et al. [30] conducted a study on sexual dimorphism in the fall armyworm, Spodoptera frugiperda, focusing on the distinguishing features between males and females. They found that male forewings exhibited a brown ground color, while females had a darker shade of brown. Additionally, the male forewing displayed a prominent longitudinal black dash at the base of the Cu vein, an indistinct reniform spot with a white v-shaped mark at the apex, a small patch of white scales at veins M3 and CuA1, and a light brown patagium (part of the thorax) with a transverse grayish-black band. In contrast, the female forewing had a less conspicuous black dash, an absence of the reniform spot except for a few white scales, no white patch at veins M3 and CuA1, and a patagium without any distinct grayish-black band.
Interestingly, the gynandromorph specimen exhibited a notable variation where the left half of the wings resembled those of a male, while the right half resembled those of a female. Similarly, the patagium on the left side resembled that of a male (prominent), while on the right side, it resembled that of a female (inconspicuous). This indicated a bilateral type of gynandromorphism. In terms of wing coupling, S. frugiperda showed sexual dimorphism in the number of frenulum, with males having a single frenulum and females having three. The gynandromorphic moth had a left half with a single frenulum and a right half with three frenula.
Furthermore, an examination of the genitalia revealed asymmetry in the genital structures of the gynandromorph. One half exhibited well-developed male genitalia structures, including a distinct uncus, valvae, aedeagus, and ampulla. The right valva was also partially developed with a distinct ampulla. On the other half, the female genitalia showed well-developed anterior apophysis, ovipositor lobes, ductus bursae, ventral plate of ostium bursae and appendix bursae, while the corpus bursae was not distinct. Based on the genitalia assessment, the gynandromorph specimen appeared to have a male-to-female proportion of approximately 60:40.
Gynandromorphs in Papilio were discovered to most frequently arise via interspecific (or intersubspecific) crosses [22]. Both polymorphic yellow and black variants can be seen in Papilio glaucus and P. alexiares Hopffer [31]. The polymorphic dark and yellow morph females are only seen in these two Papilio species, and they prominently display the color contrast in mosaicism and gyndromorphism. Scriber et al. [32] described a P. glaucus female with one golden half and one mainly dark half.
One instance of interspecific bilateral gynandromorphs was produced by mating a female Papilio glaucus with a male P. canadensis [33]. In the resulting gynandromorph, this interspecific mating brought together genes that had previously been segregated into the two gender-differentiated halves. The heterogametic female [XY (=ZW)] possessed both the X-linked suppressor (s+) gene and the Y-linked black (b+) gene of dark morph females, which resulted in the yellow (suppressed) tiger pattern for the female half. Contrast this with the interspecific (P. glaucus, P. alexiares) gynandromorph, where the female half was black, and which had the dark melanic (b+) gene and no suppressor (s-, an enablement).
The numerous enzyme activities of the melanin (black) and papiliochrome (yellow) specific pathways appeared to be coordinated with the biochemical pathways, which were temporally and spatially regulated by enzymes, including dopa carboxylase. The single major Y-linked factor on the female side of the individual coordinated all of these enzyme regulations, which had to be carried out concurrently in the same gynandromorphs [34]; however, these genes were either not expressed or absent on the male side of the individual. The activity of other sex-linked traits such as obligate diapause regulators would explain the direct development (non-diapause) of both halves of the P. glaucus/P. alexiares gynandromorph and the 1 year delay (diapause) of the P. glaucus/P. canadensis gynandromorph (with both the hemizygous female and the heterozygous male having the X-linked obligate diapause gene, od+). The distribution of sex-linked diagnostic allozymes and mitochondrial DNA variation in the two halves of such gynandromorphs may be studied in the future, but other sex-linked features, such as oviposition preferences, could not be examined [31].
11. Benefits of gynandromorphism
Studying gynandromorphs can provide valuable insights into the molecular and genetic mechanisms underlying sexual development.
Studying the sexual dimorphism can help researchers to better understand the factors that contribute to the evolutionary processes shaping the differences.
Gynandromorphs can be useful for comparative studies between sexes. By analyzing the morphology, behavior, and physiology of gynandromorphs alongside typical males and females, scientists can identify and explore the similarities and differences in these characteristics. This can provide insights into the roles of specific genes or hormones in shaping sex-specific traits.
Gynandromorphs offer a window into the intricate process of embryonic development. They provide visual evidence of how cells differentiate and interact during early development, offering valuable insights into the mechanisms involved in tissue patterning, cell signaling, and cell fate determination.
Gynandromorphs, being rare individuals, can have a special conservation value. These unique specimens can be of interest to collectors, museums, and scientific institutions, which can help raise awareness about the diversity and conservation needs of lepidopteran insects and their ecosystems.
Gynandromorphs offer unique opportunities to study the genetic basis of sexual development and sexual dimorphism.
Public engagement and education: Gynandromorphs can generate interest and curiosity about the natural world and provide opportunities for educational outreach.
12. Conclusion
The study of gynandromorphy in lepidopterans provides a fascinating glimpse into the complex world of sexual development and phenotypic variation. By examining these unique individuals with a mosaic of male and female traits, researchers have gained valuable insights into sex determination mechanisms and the modular nature of lepidopteran morphology. The occurrence of gynandromorphic mutations also sheds light on the evolvability and adaptability of lepidopteran species. Overall, this book chapter highlights the importance of gynandromorphy as a fascinating behavioral phenomenon that deepens our understanding of the intricate processes underlying the diversity and complexity of lepidopteran biology.
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Written By
Soumya Shephalika Dash and Satya Narayan Satapathy
Submitted: 13 July 2023Reviewed: 14 July 2023Published: 06 September 2023
Open access peer-reviewed chapter
