Studies on remating behaviour in the Drosophila bipectinata species complex: Intra- and interspecific variations
Introduction
Sexual selection acts on traits that influence reproductive success in both males and females (Andersson, 1994). However, such traits which may have evolved for the benefit of one sex can also incur costs in the other sex resulting in sexual conflict over mating traits. Although male reproductive traits may evolve in response to sexual selection by cryptic female choice, these traits can also impose costs to female fitness (Cordero and Eberhard, 2003). Bateman (1948) suggested that the female fitness is maximized by mating with one or few males. However, this perspective is now shifting to one in which females are thought to obtain direct phenotypic and indirect genetic benefits from multiple matings (Simmons, 2005). Moreover, the direct and indirect benefits to females exceed the costs, resulting in coevolution of these traits in both males and females (Cordero and Eberhard, 2003).
In order to attain benefits, Drosophila females frequently mate with more than one male and store the sperm from multiple males establishing the opportunity for both pre- and post copulatory sexual selection to operate. Once mated, the female is usually unwilling to accept another male for some time because of the behavioural and physiological changes that occur after mating, including decreased attractiveness to males, decreased receptivity to further mating, increased egg laying, increased risk of predation, physical harm, exposure to deleterious seminal products and decreased life span (Chapman et al., 1995, Jennions and Petrie, 2000, Baer et al., 2006, den Boer et al., 2010).
In the last few decades, evidence for intra- and interspecific variations in remating frequency and latency in Drosophila is well documented by several workers (e.g. Singh et al., 2002). The variation in female remating might be attributed to female genetic traits and/or male genetic traits affecting female remating (Harano and Miyatake, 2007). The inheritance of female and male traits related to female remating behaviour has been extensively studied in Drosophila melanogaster. In this species artificial selection revealed genetic variation in the female traits that control female remating speed (Gromko and Newport, 1988, Sgro et al., 1998). When males are left to adapt to the female phenotype in an experimental population preventing females from evolving, the ability of males to increase the rate of female remating evolved within the population (Rice, 1996). These findings suggest that the genetic variation of female and/or male traits potentially causes the difference in female remating behaviour. Similarly, Clark and Begun (1998) have shown the putative role of female genotype on both remating frequency and also the propensity of doubly mated female to use sperm from either of the males. Duration of copulation is another important component of Drosophila mating behaviour. Experimental evidence suggests that the duration of copulation is not an exclusive part of male mating activity as generally it is under control of both females and males (Hirai et al., 1999). However, in D. melanogaster, D. simulans, D. mojavensis and D. athabasca, the copulation duration is based on males (Mac Bean and Parsons, 1967, Patty, 1975, Krebs, 1991).
Remating behaviour has previously been studied to understand its causes, its effects upon the fitness of a single individual and population as a whole, the cost incurred in its evolution, and its role in sexual selection leading to speciation. Studies involving the comparison of this trait across closely related species have not yet been reported. The Drosophila bipectinata species complex, which comprises four very closely related species namely D. bipectinata (Duda, 1923), D. parabipectinata (Bock, 1971), D. malerkotliana (Parshad and Paika, 1964) and D. pseudoananassae (Bock, 1971), may prove to be an interesting model for studying and comparing this aspect of behaviour. The females of the four species are morphologically indistinguishable. However, the males can be distinguished on the basis of sex comb pattern and pigmentation of abdominal tip (Singh and Sisodia, 2008). They are known to occur in the Oriental-Australian biogeographic zones where all the four species are sympatric over parts of their range (Kopp and Barmina, 2005, Matsuda et al., 2005).
Evolutionary studies based on sexual isolation, degree of crossability, isozyme variations, polytene chromosome morphology and on the degree of divergence in nuclear and mitochondrial DNA have been done to a great extent in the members of this complex (Singh and Sisodia, 2008, Banerjee and Singh, 2012). However, extensive behavioral studies have not been done. The few examples of studies that examined behaviour looked at courtship patterns and mating behaviour in four species (Hegde and Krishnamurthy, 1979, Crossley, 1986). Therefore, the present work aims to extend those limited observations by studying aspects of remating behaviour that include remating latency, frequency and copulation duration in first and second matings across all four species of this complex. These data could improve our understanding about the adaptive evolution of this trait, and also throw light on the evolutionary relationship shared by these species, thereby furthering knowledge about mechanisms of speciation.
Section snippets
Drosophila stocks
During the present study, the following stocks of four species originating from different geographic localities in India and abroad were employed:
D. bipectinata: Pune (PN 99), India, Bodh Gaya (B. Gaya), India, Nairobi (K-aaj 072), Kenya and Kota Kinabalu (K-aaj 078), Malaysia.
D. parabipectinata: Mysore (Mys), India, Celebes (Indo), Indonesia, Los Banos (K-aam 068), Philippines and Chiang Mai (K-aam 065), Thailand.
D. malerkotliana: Raichur (RC 91), India, BHU (Banaras Hindu University),
Female remating
Chi-square test revealed significant intraspecific variation in the number of remated females among different strains of D. bipectinata (χ2 = 9.058, df = 3, P < 0.05), D. malerkotliana (χ2 = 14.86, df = 3, P < 0.01) and D. pseudoananassae (χ2 = 7.87, df = 3, P < 0.05). Fig. 1a shows comparisons for female remating frequency in different strains of four species of the D. bipectinata complex. Similarly, significant interspecific variation in number of remated females was found in four species of the complex (χ2 =
Discussion
In Drosophila, successful mating depends upon male activity and female receptivity. Females of Drosophila undergo a series of behavioral and physiological changes after mating, which lead to both short term and long term effects. The short term effect called the copulation effect in Drosophila is due to seminal fluid components transferred during mating by males (Singh et al., 2002). The ejaculatory duct protein Esterase-6 secreted from the male accessory glands causes an initial decrease in
Conclusion
Female remating is fundamental to evolutionary biology as it determines the patterns of sexual selection via sperm competition. The present study demonstrates intra- and interspecific variations in remating frequency, latency and duration of copulation in first and second matings in four species of the D. bipectinata complex i.e. D. bipectinata, D. parabipectinata, D. malerkotliana and D. pseudoananassae. Difference in the incidence of remating in the members of this complex is due to the
Acknowledgements
We thank Prof. M. Matsuda, Kyorin University, Tokyo, Japan for kindly providing the stocks of D. bipectinata species complex. Thanks are also due to Dr. Edward V. Maytin, Lerner Research Institute, Cleveland Clinic Foundation, U.S.A. for reading the manuscript critically and suggesting changes in it. The financial assistance in the form of Meritorious Fellowship to A S and UGC-BSR Faculty Fellowship Award to B N S from the University Grants Commission, New Delhi is gratefully acknowledged. We
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