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Sperm competition in Odonata (Insecta): The evolution of female sperm storage and rivals' sperm displacement
Abstract
Odonates (dragonflies) are well known for the ability of the males to displace sperm stored in the female's sperm-storage organs during copulation. By this means, copulating males are able to increase their fertilization success. This ability has been used as an example to illustrate a conflict of interests between the sexes in which males have evolved sperm-displacement mechanisms whilst females have presumably evolved means to avoid sperm displacement. The present review has four aims: (1) to describe the copulatory mechanisms used during sperm displacement; (2) to analyse the causes of sperm usage patterns; (3) to discuss this information using current hypotheses on conflict between the sexes; and (4) to illuminate topics for further research. Four copulatory mechanisms are described: sperm removal (physical withdrawal of stored sperm), sperm repositioning (‘pushing’ of rival sperm to sites where its use will be least likely), female sensory stimulation to induce sperm ejection, and sperm flushing (displacement of sperm using the copulating male's sperm). Sperm-precedence studies in Odonata are scarce and their values vary considerably between species. In those species in which sperm displacement is incomplete, the last copulating male obtains a high but variable short-term fertilization success which decreases with time. Some male and female factors affecting sperm precedence patterns are mentioned: (1) male variation in genital morphology; (2) duration of copulation influenced by the male (the longer the copulation, the more stored sperm displaced); (3) adaptations of the sperm-storage organs that allow the female to manipulate the sperm she has received (i.e. avoiding sperm displacement, re-distributing sperm masses, favouring sperm located in certain sites and ejecting sperm after copulation). We suggest that male and female odonates have co-evolved at the level of genital function with the control of stored sperm as the focus of the conflict. The benefits for males in this co-evolution lie in maximizing their fertilization success. However, it is not clear what females obtain from storing sperm and making it unreachable during sperm displacement. Two hypothetical benefits that females may obtain for which some evidence has been gathered are genetic diversity and viability genes. It is finally suggested that odonates can become excellent subjects of study for testing current ideas related to sexual conflict and speciation processes through sexual selection.
... The predaceous order Odonata is a primitive group includes both the dragonflies and damselflies, separated into three suborders [1,2] namely Anisoptera (dragonfly with eight living families), Zygoptera (damselfly with 17 living families) and Anisozygoptera which is intermediated in its morphological characteristics between the two suborders and represented by two species, one in Himalaya Mountains and another species in Japan, although only one family is now living, fossil evidence of 10 extinct families indicates considerable early diversity within this suborder [3].More than 6000 species were recorded worldwide [4]. The Anisoptera is divided into three superfamilies: Libelluloidea, Aeshnoidea and Cordulegasteroidea [5]. ...
... Schaefer et al. [11] mentioned that the male of Epiaeschna hero Fab. is largest dragonfly in the northeastern US were caught unexpectedly in traps designed to catch Calosoma sycophanta which feeds on the larvae of the gypsy moth. Aguilar et al. [2] studied the Sperm competition in Odonata and the evolution of female sperm storage and described the four copulatory mechanisms used during sperm displacement. Bouchard [12] prepared a guide to aquatic macro-invertebrates of the Upper Midwest in the United States which included some insect orders especially the Odonata (Dragonflies and Damselflies) an illustrated keys to the larvae of the families are given and mentioned that they are most abundant and diverse in standing water and all the adults and larvae are predators. ...
... (Figure: 9a, 9b): Male genitalia are the most important diagnostic characteristics used to distinguish between the different species. Many researchers [2,6,7] studied the male genitalia of species belong to this family. The male genitalia (or secondary intromittent sexual apparatus) are situated on the ventral surface of the 2 nd and 3 rd abdominal segments and consist of a deep channel or pit (the fossa) in which lie a 4-segmented tubular penis. ...
This study includes a morphological study of the Sympetrum arenicolor Jödicke, 1994 (Odonata: Libellulidae). The specimens were collected in some localities of Kurdistan region-Iraq from the period of March until November 2014. The adults described in detail, important body parts such as antenna, rostrum, male and female genitalia were illustrated. Localities and date of collecting were mentioned
... Sperm removal is another behavior that is common among odonates and insect taxa where females mate with multiple partners. Several species of odonates have "last male precedence," in which the male that was the last to mate with the female will have a high paternity success rate (C ordoba- Aguilar et al. 2003). This is due to the dual function of the odonate phallus to both displace prior sperm and to deposit sperm during copulation (Waage, 1979). ...
... This is due to the dual function of the odonate phallus to both displace prior sperm and to deposit sperm during copulation (Waage, 1979). Because of this last male precedence, male odonates often engage in extended mating times or postcopulatory mate guarding (C ordoba-Aguilar et al. 2003). To our knowledge, sperm removal has not been documented explicitly among caddisflies. ...
In a stroke of good luck for aquatic scientists and insect enthusiasts, the May 2022 Joint Aquatic Sciences Meeting (JASM) in Grand Rapids, Michigan coincided with a spectacular hatch of hydropsychid caddisflies. To estimate density, we enumerated caddisflies on 12 polarized window panels on the western face of the DeVos Place, which faced the Grand River. We found an average of 57.8 caddisflies per 2.0 Â 2.3 m window panel (density of 12.6 caddisflies m À2). We observed American robins, swallows, sparrows, and jumping spiders preying and scavenging during the hatch. We also describe here our observations of a novel precopulatory behavior in the species Hydropsyche morosa, which we describe as a "head-to-tail" position. We discuss our natural history observations and share thoughts on how conferences can be a springboard for networking and collaborative science, natural history-focused or otherwise.
... The dual function of male genitalia in sperm displacement and transfer has been predicted from the combined examination of the ultra-structures of the male and female genitalia in the Odonata [9] . It is a widespread fact that not all male genitalic structures function only in sperm transfer during the time of copulation (in copula), but that they perform copulatory courtship through movements and interactions with the female genitalia in the Diplopoda [2][3][4] . ...
... The phallopods become fully erectile when inflated by muscular action during stage II. Muscles that induce pressure changes are manifest by movements of specific structures or segments [9] . Thus there is movement of the phallopods within the female genital tract after coupling has been accomplished. ...
Not all male genitalic structures function only in sperm transfer during the time of copulation (in copula), they perform copulatory courtship through movements and interactions with the female genitalia. These structures were considered 'functional luxuries' through natural selection, mate choice and conflict of interests. The genital biomechanics of Centrobolus millipedes have examined ex copula then in copula to make actual correlations between the male and female genitalia. Two methods were employed: (1) artificial simulation of gonopod movements and (2) freeze-fixation in order to understand their functional equivalents. After copulating for approximately 10 minutes pairs were freeze-fixed by pouring liquid nitrogen (-196 °C) upon them. After one month in 70% ethanol at-10 °C, the copulatory organs were dissected from the animals under the light microscope to remove the vulva sacs and associated tissue that concealed the regions of contact. Structure-function relationships of the male accessory genitalia (gonopods) were discussed in the spirobolidan millipede genus Centrobolus and compared to julid millipedes.
... The relationship between sexual conflict and genital evolution has been reviewed recently in insects (Simmons 2014), and in-depth discussions exist for several taxa, including water striders (Arnqvist 1997), odonates (Córdoba-Aguilar et al. 2003;Cordero-Rivera and Córdoba-Aguilar 2010) and water beetles (Miller and Bergsten 2014). Therefore, here we concentrate in a few clear examples, and suggestions for future experiments. ...
... In some species, sexual conflict has apparently resulted in the evolution of aggressive copulation by males, whose intromittent organ has evolved as a wounding device, resulting in extreme sexual conflict (Reinhardt et al. 2014). The genital ligula in male odonates has a diverse form and commonly is covered by spines, which are thought to be devices to trap and remove rivals' sperm (Córdoba-Aguilar et al. 2003). However, its function as wounding devices has to be studied, and the same can be applied to other aquatic insects (i.e. the aedeagus of Dytiscus; see Guignot 1933). ...
The field of sexual selection has been historically dominated by a stereotyped view of the sexual roles, with competing males and selective females, but in recent decades there has been a paradigm switch, with the emergence and dominance of the concept of sexual conflict. Put simply, there is sexual conflict when the optimum value for a trait (or a group of traits) is different for females and males. Although the recent literature mainly considers sexual conflict as a process separate from the other well-known processes in the field of postcopulatory sexual selection (sperm competition and cryptic female choice), our approach is that sexual conflict is the consequence of several pressures related to natural and sexual selection, and not a process by itself. Therefore, here we consider sexual conflict as a part of a continuum of sexual selection mechanisms. We concentrate on the effects of sexual conflict on reproductive behaviour of three groups of aquatic insects, whose habitats differ markedly, water striders, odonates and diving beetles, but also include some examples of studies addressing sexual conflict in other groups of aquatic insects. Our hypothesis is that the dimensional structure of the habitat will affect the intensity of sexual conflict over mating rate, copulation duration and postcopulatory guarding. There is abundant evidence and comprehensive reviews of the conflict over mating rates in water striders, odonates and, to a lesser degree, diving beetles. The bi-dimensionality of the water surface allows an easy monopolisation of females by males in this microhabitat, and water striders conform to this rule, so that the commonest mating system is characterised by strong conflicts and struggles before and after copulation. For animals like odonates, which are fast fliers and can use diverse terrestrial microhabitats, the opportunities for males to force females to copulate are certainly limited. In the case of diving beetles, the situation seems more favourable for the females, as they could control male approaches by hiding easily in the vegetation, or even in the case of extreme male density they could fly away and move to a different water body. The sexual conflict over mating duration is also intense in water striders, and also relevant in the other reviewed groups. In the field of postcopulatory conflicts, odonates have offered the best examples of male adaptations and female counter-adaptations, which are even more elaborated when studying the evolution of genitalia. We end by summarising our main conclusions and propose some ideas for future work. We stress that a comprehensive understanding of sexual conflicts in animals requires the study of both male and female anatomies, as well as their behaviours, avoiding assumptions or gender stereotypes, which have historically biased research to a male-view approach.
... In this chapter we focus on this aspect. Although a more comprehensive review was written recently (Córdoba-Aguilar et al. 2003), including many ideas derived from the theories of sperm competition, we here concentrate more on lines of research where ideas of cryptic female choice (Box 15.1) and sexual con ict (Box 15.2) can be explored, while spermcompetition theories (Box 15.1) are discussed when they are relevant. ...
... This was followed by ne descriptions of similar processes in other odonates (Miller and Miller 1981; Miller 1987b ). Since then our knowledge, based on morphological and functional evidence, has revealed a complex and dynamic co-evolution between the sexes in which the female ability to store sperm from previous mates is the cornerstone for such processes (Córdoba-Aguilar et al. 2003). Males have responded to such pressure by evolving adaptations aimed to have access to a rival's stored sperm from previous matings. ...
Females may choose their male mates. However, both sexes may engage in a kind of dispute not to be coerced into mating (for females) and to be chosen (for males). These two hypotheses (called female choice and sexual conflict, respectively) are currently in vogue in studies of sexual reproduction. This chapter highlights some instances where both can be tested in odonates. These instances are: during copula invitation by males, for the duration of copulation, and during the male post-copulatory displays preceding and during oviposition. There are four other aspects that may be investigated to see the prevalence of each hypothesis: the differences of genitalic diversity across populations, the genitalic complexity at the multiple species level, the female benefits when mating with 'attractive' males, and the costs to evade superfluous matings.
... Sperm competition can occur both by preventing the female from mating again with others (via mating plugs, guarding, prolonged copulation, the induction of a refractory period in the female, etc.) and by obtaining sperm priority. Male adaptations for sperm priority comprise many behavioral and physiological components (such as sperm removal, stratification, last-in-first-out mechanisms, sperm dilution, the chemical or behavioral stimulation of the female, the evolution of particular sperm traits, etc.) [24] reported in the order Odonata [27] and in the mealworm beetle Tenebrio molitor L. [28], grasshopper Locusta migratoria L. and the tree cricket Truljalia hibinonis (Matsumura) [29,30], flies Drosophila melanogaster Meigen [31] and Dryomyza anilis Fallén [32]. As a consequence, estimating the degree of polyandry in a species involves considering the possibility of such post-mating sexual selection mechanisms [33][34][35][36] and the reproductive success advantages for the last male that mated with a female (the so-called last male sperm precedence), which is particularly common in insects. ...
The red palm weevil Rhynchophorus ferrugineus is an invasive pest from southeastern Asia and Melanesia that has spread widely across the Middle East and the Mediterranean Basin over the last 30 years. Its endophagous larvae cause huge amounts of damage to several palm tree species from the Arecaceae family. Many of these palms are economically important for agricultural and ornamental purposes. Therefore, a lot of attention has recently been focused on studying this species with the aim of identifying sustainable and effective eradication strategies. Sterile insect techniques are biological control strategies that are currently being investigated for their potential to eradicate this pest in selected invasion areas. Mating system features (e.g., polyandry and related features) can affect the success and suitability of these approaches. The main goal of this research was to assess the performance of a previously developed microsatellite panel in terms of the paternity assignment of progeny from laboratory mating experiments. Using a simulation approach, we evaluated the reliability of the microsatellite markers in the paternity tests both in complex laboratory experiment scenarios and on the progeny of wild-caught gravid females to help future studies on the RPW mating system. As a case study of the simulation results, we performed two double-mating experiments, genotyped the progeny and estimated the P2 values to compare to the expected progeny genotypes according to the crossing scheme of each experiment. The results of our simulations on laboratory experiments showed that it was possible to carry out paternity assignments for all progeny with reliable statistical confidence using our 13 microsatellites set. On the contrary the low genetic variability measured in red palm weevil populations in invaded areas made the resolution power of our loci too low to carry out paternity analyses on natural populations. Results of laboratory crossing were completely congruent with the expectations from the Mendelian laws.
... In odonates, males hover over females for 'wing display' (Cordero Rivera & Córdoba Aguilar, 2010) and hold females by head (dragonflies) and prothorax (damselflies). Thereafter, females raise abdominal tip to receive male genitalia, forming a typical 'mating wheel' (Wellenreuther & Sánchez Guillén, 2016); males displace sperms of prior males using their genitalia (Córdoba Aguilar et al., 2003). Wing pigmentation influences male-male competition (Guillermo Ferreira et al., 2019) and female mate choice (Tsubaki et al., 2010). ...
... Finally, other mechanisms act at level of ejaculate, and include sperm removal and repositioning, sperm polymorphism, or incapacitation (Table 10.2). The ability for sperm removal and repositioning has been intensively studied in the Odonata (see reviews by Córdoba-Aguilar et al., 2003;Cordero-Rivera & Cordoba-Aguilar 2010). It occurs in the oldest extant damselfly, Hemiphlebia mirabilis, suggesting that was acquired early in odonate evolution (Cordero-Rivera 2016). ...
... The genital ligula has a morphology which suggests that males use the subterminal part of this organ to remove sperm from females (e.g. Córdoba-Aguilar et al. 2003;Cordero-Rivera & Córdoba-Aguilar 2000). Further observations and experiments are needed to unravel sperm competition mechanisms in this family. ...
Odonata females are, in general, historically neglected in taxonomic descriptions in
regard to its morphology, thus, depleted from essential information such as the definition of reliable diagnostic characters that allows female identification needless of male
association. With the general objective of collaborating with the advance of female
taxonomic knowledge in the order, establishing reliable diagnostic characters and
revisiting species, this thesis had the specific objectives: revision of the Neotropical
genera Franciscobasis Machado & Bedê and Minagrion Santos; description of the
ontogenetic coloration changes in females of Ischnura capreolus; description of
unknown females with optimized diagnostic characters that allow their identification in
the absence of males; description of species new to science. The results presented here,
shed new light on the importance of diagnosing and correctly describing females in
Odonata, altering the paradigm of coloration as a diagnostic character and increasing
taxonomic information through complete morphological and integrative assessment, all
corroborated with evidence.
... mating plug formation, Wigby & Chapman, 2005;Avila et al., 2010), thereby facilitating sperm storage (Tram and Wolfner, 1999;Wigby et al., 2009;Zizzari, Smolders & Koene, 2014). Particularly in species where females mate with multiple partners, ACPs can play an important role in post-copulatory sexual selection, by affecting sperm storage, sperm digestion and sperm displacement, thereby reducing competition between rival males and increasing male reproductive success (Córdoba-Aguilar, Uhía & Cordero Rivera, 2003;Ramm, Parker & Stockley, 2005;Wigby et al., 2009;Bussiere et al., 2010). ...
Male accessory-gland proteins are known to affect female physiology in multiple ways, maximizing a
male’s reproductive success—often at a cost to the female. Due to this inherent sexual conflict, accessory
gland proteins (ACPs) are generally studied in separate-sex organisms. While ACPs have also been identified
in simultaneous hermaphrodites as an important part of post-copulatory sexual selection processes,
their study has lagged behind that of ACPs in organisms with separate sexes. In the great pond snail,
Lymnaea stagnalis, an ACP affecting egg laying, ovipostatin, is produced in the prostate gland. Based on the
published partial Ovipostatin gene sequence, we now provide the complete mRNA and gene sequences, and
confirm that gene expression is prostate gland-specific. More importantly we observed a significant increase
in Ovipostatin expression in sperm donors after ejaculation. Ovipostatin gene expression did not differ
between donors giving their ejaculate first (primary donors) and those donating an ejaculate after having
been inseminated (secondary donors). These observations support a role for ovipostatin in reproduction
and highlight the importance of standardizing the time point when measuring expression levels of ACPs.
... Some other animals, like dragonflies, use sperm removal strategies to overcome conflicts over paternity. Their copulatory organs possess small spines that trap the sperm from previous mating encounters and that allow them to remove the other males' sperm from the females' sperm storage organ before transferring their own sperm (Córdoba-Aguilar et al. 2003). All the mentioned displays provide males with advantages since they reduce malemale competition and increase their paternity success; however, for females this is not necessarily optimal (see Brennan and Prum 2012 for a discussion on this). ...
Males and females differ in their reproductive investment, resulting in what is called “sexual conflict”. In this review we start by offering a brief description of what sexual conflict is and what the important variables are that shape the way in which it is expressed (and can be measured). We subsequently analyze the causes of sexual conflict following Tinbergen’s four questions, with a special emphasis on the ontogenetic level, the latter with the specific aim to provide a more integrative view of sexual conflict and its evolution.
... To the best of our knowledge, however, no studies have been carried out to compare mating harassment rates between territorial and nonterritorial species. Furthermore, even if mating harassment rates are indeed low in territorial species, females might still benefit from being able to use stored sperm to fertilize their eggs and thereby avoid costs associated with re-mating (Córdoba-Aguilar, Uhía, & Rivera, 2003). ...
In nonterritorial damselflies, females often come in multiple color morphs, perhaps because females with rare colors experience reduced sexual harassment, and thus have a frequency‐dependent fitness advantage, compared to females of the most common color morph, but such polymorphisms are rare in territorial species. We consider three hypotheses to explain the rarity of female color polymorphisms in territorial species: (a) misdirected male aggression, (b) poor male mate recognition, and (c) low mating harassment rates. The first hypothesis has some empirical support, and can account for the absence of andromorphs (i.e., females that resemble males), but does not explain the absence of multiple heteromorphs. We tested the second hypothesis by presenting females of two novel color morphs (green‐ or red‐banded abdomens) to territorial male Hetaerina capitalis. Females of both novel color morphs elicited fewer sexual responses than control females, and the red morph occasionally elicited aggressive responses. These results indicate that novel female color morphs would experience reduced mating harassment in this species, contradicting the hypothesis that male mate recognition is too poorly developed to reduce harassment of novel female morphs. By process of elimination, the third hypothesis, that harassment rates are too low in territorial species to provide rare female morphs a fitness advantage, is favored, but remains untested. Our findings also suggest that the common practice of color‐marking odonates for behavioral research is likely to interfere with mate choice, as has long been known to be the case in birds.
... The genital ligula has a morphology which suggests that males use the subterminal part of this organ to remove sperm from females (e.g. Córdoba-Aguilar et al. 2003;Cordero-Rivera & Córdoba-Aguilar 2000). Further observations and experiments are needed to unravel sperm competition mechanisms in this family. ...
The female of Dicterias atrosanguinea Selys, 1853 is described and illustrated based on two specimens collected in Pará and Amazonas States, Brazil. We compare the female with the most closely related species, Heliocharis amazona Selys, 1853, and present SEM images of the genital ligula for both D. atrosanguinea and H. amazona males. Additionally we provide behavioral observations on D. atrosanguinea males.
... To store sperm, many species have developed dedicated structures in their reproductive tract. These structures range from more or less complex tubules (e.g., in birds: Bakst 1987;Birkhead and Møller 1992;Brillard 1993;Sasanami et al. 2013;Holt and Fazeli 2016 and some reptiles: Pearse and Avise 2001;Han et al. 2008) to highly sophisticated organs containing multiple compartments (Eberhard 1985(Eberhard , 1996 e.g., the spermathecae of amphibians : Sever 1991: Sever , 1997: Sever , 2002insects: Bloch Qazi et al. 1998;Baer et al. 2006;Córdoba-Aguilar et al. 2003 andgastropods: Baminger andHaase 1999;Koemtzopoulos and Staikou 2007;Whelan and Strong 2014;annelids: Novo et al. 2013). Interestingly, large interspecific divergence in morphology, size, complexity, and even number of these organs have been reported. ...
In the majority of internally fertilizing animals, females are equipped with sperm storage organs where they store the sperm received during copulation. In many simultaneously hermaphroditic pulmonates, these organs consist of complex spermathecae that show inter- and intra-specific variation in their structure. This variability is theoretically predicted by postcopulatory sexual selection in the context of sperm competition and cryptic female choice. In this study, the variation in the structure of the spermatheca was investigated in the land snail Helix aperta from four natural populations near Bejaia in northern Algeria. The populations were different in local snail density, probably also reflecting the intensity of sperm competition. We tested whether the spermatheca showed differences that are predicted by sperm competition theory. In addition, we tested whether the spermathecal structure depends on the shell size and/or is correlated with other reproductive organs that are thought to be affected by sexual selection. We found that the fertilization pouch of H. aperta consists of a simple fertilization chamber and 3–9 spermathecal tubules. The four populations did not differ significantly in the mean number of these tubules. However, significant differences were found in the length of the main tubule, the length of the fertilization chamber, and the average length of lateral tubules. In addition, strong associations were detected between the lengths of these structures and the local snail density, while no effect of shell size or reproductive organs was found. Our results indicate that the intensity of sperm competition may not affect the total number of spermathecal tubules, but may increase their lengths. This increase in spermathecal length may reflect an improved sperm storage capacity that is probably beneficial in situations of high sperm competitions intensity.
... So a male removes sperm of previous mates before he transfers his own sperm. Since its discovery, sperm competition has been recorded in many other odonates (Miller & Miller 1981; Miller 1987; Cordero et al. 1995), and theories of co-evolution between the sexes were advanced, suggesting that the end result of such an elaborative shape of male penis is the ability of the females to store sperm from previous matings (Córdoba-Aguilar et al. 2003). The finding of Waage (1979) opened a new field of research on reproductive behaviour and sexual selection that has been explored thoroughly afterwards in other taxa (Simmons 2001). ...
The field of odonatology has developed considerably during the past century. Three figures, namely E. Selys-Longchamps, R.J. Tillyard and P.S. Corbet, have undisputedly founded our current knowledge of odonatology and contributed massively to the understanding of systematics, biology, ecology and behaviour of odonates. The year 2017 will mark the 100th anniversary of Tillyard's The Biology of Dragonflies. We review the book and the author's life and contributions to Australian odonatology. We present an updated history of odonatology and highlight prominent advances in the field. The influence of the book on non-scientists is described. Future research in odonatology on aspects that have not been studied and others that need further investigations are discussed.
... None of the birch females mated to willow males had sperm in the bursa and spermathecae when dissected immediately after mating. The lack of sperm in heterospecifically mated birch females seems to be caused by the failure to transfer sperm rather than other mechanism such as expelling sperm caused by females following insemination, a process that has been documented in several insect species (Corderos and Miller 1992; Córdoba-Aguilar et al. 2003). This can act as one of the early barriers to gene flow, which substantially prevents gene flow in the heterospecific crosses between birch females and willow males. ...
One of the major goals in speciation research is to understand which isolation mechanisms form the first barriers to gene flow. This requires examining lineages which are still in the process of divergence or incipient species. Here, we investigate the presence of behavioural and several cryptic barriers between the sympatric willow and birch host races of Lochmaea capreae. Behavioural isolation did not have any profound effect on preventing gene flow. Yet despite pairs mating indiscriminately, no offspring were produced from the heterospecific matings between birch females and willow males due to the inability of males to transfer sperm to females. We found evidence for differences in genital morphology which may contribute to failed insemination attempts during copulation. The heterospecific matings between willow females and birch males resulted in viable offspring. Yet fecundity and hatchability was remarkably reduced, which is likely the result of lower efficiency in sperm transportation and storage and lower survival of sperm in the foreign reproductive tract. Our results provide evidence for the contribution of mechanical and several postmating-prezygotic barriers which predate behavioral isolation and act as primary inhibitors of gene flow in this system. This is a surprising, yet perhaps often overlooked feature of barriers acting early in sympatric speciation process. This article is protected by copyright. All rights reserved
... Detecting no phylogenetic correlation between female internal genital and body sizes suggests that these traits are under different selection pressures. In spiders, female body size is generally believed to be under strong positive fecundity selection [38] , whereas female genitalia may respond to diverse aspects of sexual selection [35, 52, 53], or to natural selection that counters genital misfits [35]. On the other hand, we detected a positive correlation between male non-intromittent genital size and male body size, implying that the same selection pressures that act on male size also drive the size of non-intromittent part of the genitalia. ...
Background
In most animal groups, it is unclear how body size variation relates to genital size differences between the sexes. While most morphological features tend to scale with total somatic size, this does not necessarily hold for genitalia because divergent evolution in somatic size between the sexes would cause genital size mismatches. Theory predicts that the interplay of female-biased sexual size dimorphism (SSD) and sexual genital size dimorphism (SGD) should adhere to the ‘positive genital divergence’, the ‘constant genital divergence’, or the ‘negative genital divergence’ model, but these models remain largely untested. We test their validity in the spider family Nephilidae known for the highest degrees of SSD among terrestrial animals. ResultsThrough comparative analyses of sex-specific somatic and genital sizes, we first demonstrate that 99 of the 351 pairs of traits are phylogenetically correlated. Through factor analyses we then group these traits for MCMCglmm analyses that test broader correlation patterns, and these reveal significant correlations in 10 out of the 36 pairwise comparisons. Both types of analyses agree that female somatic and internal genital sizes evolve independently. While sizes of non-intromittent male genital parts coevolve with male body size, the size of the intromittent male genital parts is independent of the male somatic size. Instead, male intromittent genital size coevolves with female (external and, in part, internal) genital size. All analyses also agree that SGD and SSD evolve independently. Conclusions
Internal dimensions of female genitalia evolve independently of female body size in nephilid spiders, and similarly, male intromittent genital size evolves independently of the male body size. The size of the male intromittent organ (the embolus) and the sizes of female internal and external genital components thus seem to respond to selection against genital size mismatches. In accord with these interpretations, we reject the validity of the existing theoretical models of genital and somatic size dimorphism in spiders.
... In the case of cryptic female choice, copulatory movements of the intromittent organ against female genital tissues are thought to trigger physiological responses in the female that enhance male fertilization success (Eberhard 1996). Female promiscuity also sets the stage for male–male competition inside the female genital tract—where, for example, intromittent organs may actively remove semen left behind by earlier mates (Cordoba-Aguilar et al. 2003; Wada et al. 2010) or induce females to eject previous sperm (Tajima and Watanabe 2014). Morphological differences among copulatory organs that affect a male's ability to carry out these cryptic functions could produce differential outcomes for paternity. ...
Intromittent organs are structures that enter the female genital tract and deposit sperm; these organs are found in many animal taxa that use internal fertilization. Despite their shared function, they are fantastically diverse morphologically. Many of their species-specific shape differences are likely the result of sexual selection and coevolution between male and female reproductive tracts, but a growing number of studies have identified other factors that can also affect their functional anatomy. In this symposium, we united scientists who combine morphological methods with contemporary molecular, phylogenetic, and imaging techniques to study the reproductive performance of intromittent organs in invertebrate and vertebrate model systems. The result was a collection of studies discussing competing selective pressures that act on these structures, including the effects of life history, genes and development, sexual conflict, ecological interactions, the biomechanics of copulation, and phenotypic plasticity. There was also an overwhelming consensus that a full understanding of intromittent organ evolution will not be possible without complimentary studies of morphology and function in female reproductive tracts.
... This positioning was confirmed in one pair preserved in copula. In all Zygopteran species so far studied, stage I is used to remove sperm from previous matings and stage II to inseminate (Córdoba-Aguilar, Uhía & Cordero-Rivera, 2003). My results are compatible with this scenario also for H. mirabilis. ...
Postcopulatory sexual selection may favour mechanisms to reduce sperm competition, like physical sperm removal by males. To investigate the origin of sperm removal, I studied the reproductive behaviour and mechanisms of sperm competition in the only living member of the oldest damselfly family,
Hemiphlebia mirabilis
, one species that was considered extinct in the 1980s. This species displays scramble competition behaviour. Males search for females with short flights and both sexes exhibit a conspicuous “abdominal flicking”. This behaviour is used by males during an elaborate precopulatory courtship, unique among Odonata. Females use a similar display to reject male attempts to form tandem, but eventually signal receptivity by a particular body position. Males immobilise females during courtship using their legs, which, contrarily to other damselflies, never autotomise. Copulation is short (range 4.1–18.7 min), and occurs in two sequential stages. In the first stage, males remove part of the stored sperm, and inseminate during the second stage, at the end of mating. The male genital ligula matches the size and form of female genitalia, and ends by two horns covered by back-oriented spines. The volume of sperm in females before copulation was 2.7 times larger than the volume stored in females whose copulation was interrupted at the end of stage I, indicative of a significant sperm removal. These results point out that sperm removal is an old character in the evolution of odonates, possibly dating back to the Permian.
... Sperm precedence is said to occur if the last male to mate with a female fathers most of her eggs. It is often mechanistically based on the last male's ability to displace sperm from the spermatheca, or to redistribute it so that his own sperm are more likely to fertilise eggs, as occurs in Odonata (Cordoba-Aguilar et al., 2003). We have tested the possibility that aphids exhibit sperm precedence (Doherty & Hales, 2002, Doherty et al., 2004 ). ...
When investigating sexual strategies of aphids, it is necessary to set up multiple replicates to compensate for the small number of eggs laid per female. Genetic variation among replicates can be minimised if members of the same clone are used, but problems can arise unless the participants are also physiologically equivalent. A series of experiments on Myzus persicae (Sulzer) was performed to investigate aspects of male maturation and semen transfer that should be considered in planning or interpreting experiments on aphid sexual strategies.
... The evolutionary consequences of variation in primary male genital structures have been deduced in several taxa by studying intraspecific natural variation in morphology. The results of these experiments are consistent with postcopulatory sexual selection as the predominant force that appears to drive the evolution of primary genital morphology (e.g., Arnqvist et al. 1997; C ordoba-Aguilar et al. 2003; House and Simmons 2003; Stockley et al. 2013; Simmons 2014; Simmons and Firman 2014). Recent advances in technology have also made it possible to directly test the reproductive consequences of variation in genital morphology. ...
The genitalia of internally fertilizing taxa represent a striking example of rapid morphological evolution. Although sexual selection can shape variation in genital morphology, it has been difficult to test whether multiple sexual selection pressures combine to drive the rapid evolution of individual genital structures. Here, we test the hypothesis that both pre- and postcopulatory sexual selection can act in concert to shape complex structural variation in secondary genital morphology. We genetically modified the size and shape of the posterior lobes of Drosophila melanogaster males and tested the consequences of morphological variation on several reproductive measures. We found that the posterior lobes are necessary for genital coupling and that they are also the targets of multiple postcopulatory processes that shape quantitative variation in morphology, even though these structures make no direct contact with the external female genitalia or internal reproductive organs during mating. We also found that males with smaller and less structurally complex posterior lobes suffer substantial fitness costs in competitive fertilization experiments. Our results show that sexual selection mechanisms can combine to shape the morphology of a single genital structure and that the posterior lobes of D. melanogaster are the targets of multiple postcopulatory selection pressures.
... The sperm storage organ is physically not accessible for mating partners. In contrast to studies on sperm displacement in insects (e.g., C ordo- Aguilar et al. 2003; Xu and Wang 2010) or a flatworm (Marie-Orleach et al. 2014 ), there is, to our knowledge, no information on sperm displacement in stylommatophoran land snails. Secondly, the level of multiple paternity in progenies estimated for every snapshot moment of the season reflects the minimum mating frequency. ...
In a seasonal environment, the suitable time window for females to reproduce is restricted by both environmental conditions and the availability of males. In simultaneous hermaphrodites, which are female and male at the same time, selection on a trait that is solely beneficial for one sexual function cannot occur independently. Therefore, it is assumed that the optimal time window for reproduction is a compromise between the two sexual functions in simultaneous hermaphrodites, mediated by environmental conditions. We examined seasonal patterns of reproduction and the resulting paternity in a natural population of the simultaneously hermaphroditic land snail Arianta arbustorum. Adult and premature individuals (snails in a short protandric phase) were collected on four occasions over the entire active season. The snails were allowed to deposit eggs after which we assessed the level of paternity in their hatched offspring. Individuals mated throughout the reproductive season, whereas egg production – the major task of the female function – was restricted to the first half of the season. Snails collected in autumn were allowed to hibernate under laboratory conditions. As a result, we found that premature individuals began to mate late in the reproductive season, but did not start to produce eggs before emerging from hibernation. Our results demonstrate a temporal shift of reproductive activities; the egg production and oviposition occur mainly in the first half of the season, while sperm production and mating occur over the entire season. In subadult and adult snails, sperm obtained from several partners in the second part of the reproductive season are stored during hiberna-tion for the fertilization of eggs in the successive years. These results extend our understanding of the influence of both natural and sexual selection on reproductive strategies in hermaphrodites.
Long‐term sperm storage by females in various regions of the oviduct is documented across many invertebrate and vertebrate species. Although, many reports emphasize on the histology, histochemistry and ultrastructural features of sperm storage, very little is known about the mechanisms underlying the sperm storage. The current review documents the occurrence of sperm storage by females in a wide array of invertebrate and vertebrate species. This review also provides an insight on the presence of various molecular factors of the sperm storage tubules presumably responsible for the prolonged sperm storage with an emphasis on a model reptile, the Indian garden lizard, Calotes versicolor which contains a unique approximately 55‐kDa protein in its utero‐vaginal lavage and found to inhibit washed epididymal sperm motility in a concentration and time‐dependent manner in a reversible fashion. Indian garden lizard (Calotes versicolor) exhibits sexual dimorphism and asynchronous reproductive cycle. This necessiates female to store sperm in the uterovaginal junction (UVJ) for further use. We isolated an approximately 55‐kDa protein from UVJ which when added exogenously to sperm retards the motility in a reversible manner. Current review summarizes the factors involved in sperm storage.
Insect tagmata are often simplified and assigned to a specific functionality: head (perception), thorax (movement), and abdomen (reproduction). However, in insects generally, all body regions show elaborate functionalities of very different kinds, often down to the nanometer level. It is likely that each part of the insect body provides a (multi)functional specialization. This chapter attempts to tackle the latest achievements in our understanding of functional morphological adaptations in both adult and larval odonates: from the head-arrester-system in adults to the predatory strike of the larvae; from the unique wings to the importance of the legs in the larval stage; and from the head–abdomen interlocking during mating to the swimming abilities of the aquatic larvae. It also attempts to highlight gaps of knowledge for potential future research where young odonatologists can (and should!) enter the field. Further on, functional singularities and curiosities of Odonata are described (as variations of the standard often hold new principles) to showcase the group describe some oup of Odonata as being fascinating model-organisms for functional and biomechanical research. This perspective often yields insights into unique solutions to cope with a constantly changing environment from one of the oldest insect orders.
In odonates, male coloration is often more conspicuous than female coloration. This difference is frequently attributed to the role of male colour in male–male competition to access females. However, there are sexually dimorphic odonate species, such as the damselflies Argia hasemani and Argia croceipennis, in which male–male interactions are much less intense. In these species, it might be that male coloration affects male success directly when interacting with females. Therefore, we hypothesized that males with more intense coloration present higher copulation success. To investigate this hypothesis, we registered which males copulated in the field during 4 days and estimated the coloration of all observed males in the female visual spectrum. Surprisingly, we found that dull males had higher chances of copulation in A. hasemani, whereas in A. croceipennis male coloration did not influence the chances of copulation. Our data also indicated that brighter males of A. hasemani were also more conspicuous to potential avian predators, whereas this was not the case in A. croceipennis. We suggest that females of A. hasemani might avoid brighter males owing to increased risk of predation during copulation.
In many animal phyla, females have a unique sperm storage organ (SSO). Post-copulatory sexual selection is a powerful driving force of SSO evolution. SSOs are generally considered to have evolved through sexual antagonistic coevolution between male genitalia and the SSO and/or cryptic female choice (CFC). In cephalopods, sperm transfer and fertilization are conducted through complex processes, and sperm storage methods show inter-species variation. In some species, males implant spermatangia superficially under the female skin, and then sperm released from the spermatangia are transferred into a seminal receptacle (SR). Deep-sea cephalopods, which lack a SR, have instead evolved a deep-implanting method by which the spermatangium is embedded deep in the musculature of the mantle wall of the female. In some species, the female stores whole spermatangia within a spermatangium pocket. Because the males of most species do not insert an intromittent organ into the female when transferring sperm, SSO evolution may have been influenced by CFC alone. This review summarizes the sperm storage methods and the mechanisms of post-copulatory sexual selection in cephalopods and it is proposed that these diverse methods evolved as adaptive mechanisms through post-copulatory sexual selection.
We described and compared the mating behavior and morphology of the reproductive system in chromodorid nudibranchs, then, examined how extensively the unique usage of the penis (autotomy and sperm removal) evolved among Chromodorids. In addition to Ardeadoris egretta, all of examined five species in Glossodoris autotomized their penises at the last stage of copulation. An interspecific difference was seen in penis autotomy in Noumea and Goniobranchus. A spiral structure was recognized in the vas deferens of autotomized species. This structure is supposed to be undifferentiated “next penises” stored in the vas deferens, which ensure successive copulation in autotomized species. Though the basic mechanism of penis replenishment was consistent, the reason to autotomize their penises may not be the same. Goniobranchus reticulatus is reported to remove sperm already stored in the mating partner’s sperm storage organ(s) with backward-pointing spines on the surface of its penis. Contrary to G. reticulatus, all of ten species that autotomized their penises in the present study did not have thorny but smooth penises. When they autotomized their penises, the tip of the penises still remained in the vagina of the partners. This suggests that autotomized penises in these nudibranchs function as a kind of copulatory plugs.
Postcopulatory sexual selection may favour mechanisms to reduce sperm competition, like physical sperm removal by males. To investigate the origin of sperm removal, I studied the reproductive behaviour and mechanisms of sperm competition in the only living member of the oldest damselfly family, Hemiphlebia mirabilis , one species that was considered extinct in the 1980s. This species displays scramble competition behaviour, whose males search for females with short flights and both sexes exhibit a conspicuous “abdominal flicking”. This behaviour is used by males during an elaborate precopulatory courtship, unique among the Odonata. Females use a similar display to reject male attempts to form tandem, but eventually signal receptivity by a particular body position. Males immobilise females during courtship using their legs, which, contrarily to other damselflies, never autotomize. Copulation is short (range 4.1-18.7 min), and has two stages. In the first stage, males remove part of the stored sperm, and inseminate during the second stage, at the end of mating. The examination of genitalia indicates that males have two horns covered by back-oriented spines, which match the size and form of female genitalia. The volume of sperm in females after copulation was 2.8 times larger than the volume stored in females whose copulation was interrupted at the end of stage I, indicative of a significant sperm removal. These results point out that sperm removal is an old character in the evolution of odonates, probably dating back to the Permian.
Postcopulatory sexual selection may favour mechanisms to reduce sperm competition, like physical sperm removal by males. To investigate the origin of sperm removal, I studied the reproductive behaviour and mechanisms of sperm competition in the only living member of the oldest damselfly family, Hemiphlebia mirabilis , one species that was considered extinct in the 1980s. This species displays scramble competition behaviour, whose males search for females with short flights and both sexes exhibit a conspicuous “abdominal flicking”. This behaviour is used by males during an elaborate precopulatory courtship, unique among the Odonata. Females use a similar display to reject male attempts to form tandem, but eventually signal receptivity by a particular body position. Males immobilise females during courtship using their legs, which, contrarily to other damselflies, never autotomize. Copulation is short (range 4.1-18.7 min), and has two stages. In the first stage, males remove part of the stored sperm, and inseminate during the second stage, at the end of mating. The examination of genitalia indicates that males have two horns covered by back-oriented spines, which match the size and form of female genitalia. The volume of sperm in females after copulation was 2.8 times larger than the volume stored in females whose copulation was interrupted at the end of stage I, indicative of a significant sperm removal. These results point out that sperm removal is an old character in the evolution of odonates, probably dating back to the Permian.
In organisms in which individuals mate multiply, knowledge of the proportion of offspring sired by the last male to mate (P2) under field conditions is important for a thorough understanding of how sexual selection works in nature. In many insect groups, pronounced intraspecific variation in P2 is commonplace. Interestingly, however, in stark contrast to these observations, compilation of P2 data in dragonflies and damselflies (Odonata) indicates that a high P2, seldom below 0.95, is a feature of this taxon. Here we used double digest restriction-site associated DNA sequencing to generate a panel of single nucleotide polymorphisms (SNPs) with which we could determine paternity and estimate values of P2 in the offspring of 19 field-collected pairs of the emerald damselfly Lestes sponsa. We also estimated the relationship between P2 and male genital shape of 16 males using geometric morphometric analysis. P2 was variable (range = 0.0–1.0; mean = 0.5), and there was a marginally non-significant (P = 0.069) relationship between genital shape and P2, suggesting that males with a high P2 had an aedeagus with a broader tip. We suggest that the high P2-values reported in past studies in Odonata are partly due to the methods used to infer paternity. Use of SNPs to determine patterns of paternity and P2 in odonates is needed for a better appraisal of fitness in odonates, and would open many future avenues for use of odonates as models of sexual selection.
Background
Postcopulatory sexual selection is very important in species with reproductive strategies that involve multiple mating and prolonged sperm storage. The sperm storage organ has been hypothesized to evolve in response to different levels of sperm competition in several species while population density has been considered as a factor that approximates sperm competition risk and intensity in the field. Apart from population density, local microclimatic conditions may also play a role in determining sperm competition levels in natural populations of land snails by affecting their chances of encountering mates. The goal of this study was to investigate the variation of the structure of the sperm storage organ in the simultaneously hermaphroditic land snails Helix lucorum and Cepaea vindobonensis occurring sympatrically in two sites which differed in habitat humidity. The populations of both species from the two sites, also differed in density and in duration of reproductive period. Multiple samples were taken from each population in order to test for temporal variation.
Results
In both species, the spermatheca consisted of a simple fertilization chamber and a variable number of lateral tubules. The length of the spermatheca showed no temporal or spatial differentiation nor did it show any correlation with snail size. The number of tubules in Helix lucorum ranged from five to sixteen and in Cepaea vindobonensis from one to eight and in both species a significant difference of this trait between the two study sites was detected. In Cepaea vindobonensis, the difference in tubule number led to difference of the total tubule length which reflects sperm storage capacity of the spermatheca but this was not the case with H. lucorum in which no increase in total tubule length was detected.
Conclusions
Intraspecific variation in the spermatheca was observed in both snail species studied. The variation observed was independent of snail size, and reproduction status, while the two species responded differently to higher sperm competition levels.
Simultaneous hermaphroditism is, at least initially, favoured by selection under low density — and therefore it can be assumed that sperm competition has little importance in this sexual system. However, many simultaneously hermaphroditic nudibranchs have both an allo-sperm storage organ (the seminal receptacle) and an allo-sperm digesting organ (the copulatory bursa), suggesting the possibility of the occurrence of sperm competition. A nudibranch, Chromodoris reticulata, autotomizes its penis after every copulation and replenishes it within about 24 h to perform another copulation. We observed that the surface of the autotomized penis was covered with many backward-pointing spines and that a sperm mass was often entangled on the spines. This suggests that the nudibranch removes sperm that is already stored in a mating partner’s sperm storage organ(s) with its thorny penis. Using six microsatellite markers, we determined that the sperm mass attached to the penis were allo-sperm originating from individual(s) that had participated in prior copulations. We revealed that C. reticulata performed sperm removal using the thorny penis. These results suggest that competition in fertilization is quite intense and mating frequency in the wild is relatively high in this species.
Sexual conflict is a pervasive evolutionary force that can reduce female fitness. Experimental evolution studies in the laboratory might overestimate the importance of sexual conflict since the ecological conditions in such settings typically include only a single species. Here, we experimentally manipulated conspecific male density (high or low) and species composition (sympatric or allopatric) to investigate how ecological conditions affect female survival in a sexually dimorphic insect, the banded demoiselle (Calopteryx splendens). Female survival was strongly influenced by an interaction between male density and species composition. Specifically, at low conspecific male density, female survival increased in the presence of heterospecific males (C. virgo). Behavioural mating experiments showed that interspecific interference competition reduced conspecific male mating success with large females. These findings suggest that reproductive interference competition between con- and heterospecific males might indirectly facilitate female survival by reducing mating harassment from conspecific males. Hence, interspecific competitors can show contrasting effects on the two sexes thereby influencing sexual conflict dynamics. Our results call for incorporation of more ecological realism in sexual conflict research, particularly how local community context and reproductive interference competition between heterospecific males can affect female fitness.
We report cases of long-distance dispersal in Odonata, some of which were directly observed by identifying single individuals of riverine species in unsuitable habitat, mostly desert, far distant from reproduction habitats. The shortest possible linear distances of the observation points to reproduction habitats were measured. Furthermore, established populations of riverine species were recorded in artificial lakes in central and southern Namibia far distant from the next regular reproduction sites. Our records demonstrate that single individuals of riverine species were probably covering distances of several hundred kilometres over arid landscape without any intervening possible reproduction habitat. Although it is likely that only small numbers of individuals of the river populations may disperse long distances, relatively recent colonizations of artificial habitats suggest that a few, or even single, dispersing individuals may lead to large-scale-range expansions.
In polyandrous mating systems, sperm competition and cryptic female choice (CFC) are well recognised as post-copulatory evolutionary forces. However, it remains challenging to separate CFC from sperm competition and to estimate how much CFC influences insemination success because those processes usually occur inside the female's body. The Japanese pygmy squid, Idiosepius paradoxus, is an ideal species in which to separate CFC from sperm competition because sperm transfer by the male and sperm displacement by the female can be observed directly at an external location on the female's body. Here, we counted the number of spermatangia transferred to, removed from, and remaining on the female body during single copulation episodes. We measured behavioural and morphological characteristics of the male, such as duration of copulation and body size. Although males with larger body size and longer copulation time were capable of transferring larger amounts of sperm, females preferentially eliminated sperm from males with larger body size and shorter copulation time by spermatangia removal; thus, CFC could attenuate sperm precedence by larger males, whereas it reinforces sperm precedence by males with longer copulation time. Genetic paternity analysis revealed that fertilisation success for each male was correlated with remaining sperm volume which is adjusted by females after copulation. This article is protected by copyright. All rights reserved.
Correspondence: L. R. Dougherty, Centre for Evolutionary Biology, School of Animal Biology, The University of Western Australia, Crawley, Western Australia 6009, Australia.
The study was conducted at the Dos Bocas stream nr Santiago de Cuba, during Aug.-Sept. 2007 (30 d) and in May 2008 (5 d). ♂ ♂ are territorial, defending perching sites and returning to the same place for several days. Sperm translocation lasted about 9 s and copulation about 7.3 min. It consisted of 2 stages, recognized from the position and movements of ♂'s abdomen. Stage I took ca 6.6 min and is probably associated with sperm removal. Stage II lasted about 41.3 s, involving probably sperm transfer. Oviposition lasted for just over 1 h; the male guarding his mate during ca 30 min, whereafter he returned to his perch.
According to the movements of the o♂ abdomen, the copulation process in I. asiatica is divided into 3 stages (I, II and III). The mean duration of each stage was 75.8 ± 8.8 min, 6.4 ± 0.3 min and 15.8 ± 0.9 min for stage I, II and III, respectively (S.E.). No sperm transfer was found during stage I. The prolonged duration in stage I was related to the time of onset of copulation. Sperm was transferred into the bursa copulatrix during stage II. Although stage III was a phase without apparent abdominal movement, the sperm transfer was continued, following the sperm migration from the bursa copulatrix to the spermatheca. Immediately after copulation termination, the estimated number of sperm was 64,500 + 4,425 in the bursa copulatrix and 43,143 ± 6,397 in the spermatheca (S.E.). The role of each stage in copulation will be discussed from the viewpoint of sperm competition.
The male Ischnura asiatica (Brauer, 1865) has a pair of horns on its penis head. Because each horn is shorter than the spermathecal duct, the spermatheca is inaccessible to the male. Thus, males can not directly displace spermathecal sperm using the horns. Nevertheless during copulation displacement of sperm from the spermatheca does occur. By stimulating vaginal sensilla that communicate the presence of an egg to the muscles surrounding the sperm storage organs, sperm ejection can be induced as fertilization is anticipated by the female. Males with a large penis head might be better adapted to stimulate the sensilla and displace more sperm than those with a small penis head. From the viewpoint of females, on the other hand, there are costs if complete sperm displacement occurs. Decreasing the number of sensilla might make it difficult for the males stimulation to displace spermathecal sperm, especially where a population includes males with a large penis head. To test this hypothesis, the width of the penis head and the number of sensilla were measured in several local populations, with different body sizes, distributed in mainland Japan. The number of sensilla decreased with the width of the penis head. Therefore, a low number of sensilla in the females might be a counter- Adaptation against the male sensory stimulation.
The ♀ sperm storage organs of I. asiatica include the bursa copulatrix and the sper-matheca. The spermatheca is joined to the base of the bursa copulatrix by a sperma-thecal duct. At the tip of the ♂'s secondary genitalia, there is a pair of horns which might be used to remove sperm from the ♀ sperm storage organs. Since each horn of the ♂ genitalia is shorter than the spermathecal duct, the spermatheca might be inaccessible to ♂ ♂. However, sperm reduction occurs both in the bursa copulatrix and in the spermatheca during copulation. This suggests an alternative mechanism by which the ♂ can cause a decline in the spermathecal sperm. In order to investigate the mechanism of sperm reduction, an interrupted copulation experiment was conducted in the field. The extent of sperm reduction in the spermatheca was related to the width of the head of the secondary genitalia of the mated ♂.♀ ♀ have mechano-receptive sensilla which communicate the presence of an egg to the muscles surrounding the sperm storage organs for fertilization. Therefore, the head of the secondary genitalia might mimic the movement of the egg that stimulates the sensilla to induce spermathecal sperm ejection by the ♀.
Spermatozoan dynamics in the ♂ sperm storage organs of I. asiatica were examined with interrupted copulation experiments in the field. The copulation process was divided into 3 stages (I, II and III) according to the movements of the ♂ abdomen. ♀ ♀ interrupted just after the termination of stage I of copulation contained a much lower number of spermatozoa, both in the bursa copulatrix and in the spermatheca, than solitary ♀ ♀ captured before being attached by ♂ ♂. At the tip of the ♂'s secondary genitalia, there was a pair of horns which might be used to remove sperm from the bursa copulatrix and the spermatheca during copulation. The latter was joined to the base of the former by a spermathecal duct. Since each horn of the ♂ genitalia was significantly shorter than the spermathecal duct, the spermatheca might be inaccessible to ♂ ♂. The actual position of the horns in the ♀ sperm storage organs during stage I of copulation was observed by freezing copulating pairs using quick-freeze aerosol sprays. The horns were in the bursa copulatrix, but no horns had entered the spermatheca. Additional mechanisms of sperm removal from the spermatheca are proposed.
During copulation, Ischnura asiatica (Brauer, 1865) males remove the sperm of the females' previous mates from the spermatheca by stimulating vaginal sensilla thereby inducing sperm ejection. Because a wider penis head stimulates the vaginal sensilla more intensely, larger males with wider penis heads can remove much more sperm from the spermatheca. There are two distinct body sizes for spring (large) and summer (small) generations of I. asiatica. In the present study we show that in spring, males have wider penis heads and females have a higher number of vaginal sensilla as compared to summer adults, suggesting that mating males remove more spermathecal sperm in spring than in summer. However, interrupted copulation experiments showed that females of the spring generation had a higher number of spermatozoa in both sperm storage organs than those of the summer generation. Solitary females of the spring generation also had higher numbers of spermatozoa stored than those of the summer generation, suggesting that spring females might have larger sperm storage organs than summer females. Although the removal rate of bursal sperm was almost the same between generations, the removal rate of spermathecal sperm in the summer generation was slightly higher than that in the spring generation. Consequently, spermatozoa derived from previously mated males have a higher probability of remaining in the sperm storage organs in spring-than in summer-generation females. The size of sperm storage organs in females might be critical to understanding sperm displacement. This aspect of female anatomy has not been previously considered in studies of sperm competition in odonates.
CHAPTER SUMMARY Frogs and salamanders, the two most diverse lineages of amphibians, differ significantly in reproductive mode, morphology, and behavior. We review reproductive tactics in these lineages and consider their distribution among taxa in light of phylogeny, ecology, and organismal traits. Together these groups show a surprising diversity of alternative reproductive phenotypes that can roughly be divided into two classes: those that increase an individual’s chance of mate acquisition (e.g., satellite or intercepting males) and those that directly increase fertilization success (e.g., spermatophore capping, clutch piracy, or multimale spawning). Our survey underscores the fact that mode of fertilization (internal or external) and operational sex ratios at breeding aggregations have important implications for the frequency and nature of alternative reproductive tactics. However, our understanding of the evolution of amphibian alternative reproductive tactics is hampered by a lack of detailed information for many species. For example, most alternative tactics have been described in temperate amphibians despite the fact that tropical species account for most of the taxonomic, morphological, behavioral, and ecological diversity in this group. A challenge for future studies will be to further describe and categorize the diversity of reproductive tactics in amphibians to uncover general patterns within and across lineages in the factors that modulate polymorphism in reproductive phenotypes. INTRODUCTION In the last few decades, organismal evolutionary biologists have become increasingly aware of inter-individual differences in mate acquisition abilities that may underlie the evolution of alternative strategies or tactics for reproductive success (Shuster and Wade 2003). © Cambridge University Press 2008 and Cambridge University Press, 2009.
Mate-choice copying is a fascinating and widespread mate-choice strategy. Individuals gather public information about potential mates by observing others during sexual interactions and choose or reject the same individual as a mate as the observed individual did before. The influence of copying behavior on an individual’s mate choice can be so strong that socially acquired information can override genetically based preferences for certain phenotypes. Thus, mate-choice copying enforces dynamic processes in sexual selection. Here, we review the current state of research on mate-choice copying and focus on sex-specific aspects. We present evidence that mate-choice copying can support the evolution of novel sexual ornaments, and we discuss potential costs of mate-choice copying when public information is not reliable. Moreover, we discuss the conflict faced by males that copy since mate-choice copying increases sperm competition. In conclusion we suggest interesting topics for future research in mate-choice copying.
Cryptic female choice (CFC)
does not necessarily involve discriminative responses in the female nervous system to sperm from multiple mates. Even without any active sperm-choice mechanisms, polyandrous females can gain genetic benefits
by having an arena in which genetically superior sperm are “automatically” sorted. In this chapter, possible mechanisms in this CFC category, termed “indirect CFC
,” are reviewed. A simple theoretical model is developed to examine the hypothesis that females obtain genetic benefits by allowing only partial displacement of stored sperm by subsequent mates. The model predicts that such restricted sperm displacement automatically grants genetic benefits when genetically superior males copulate more times per encounter with the female than less fit males. The promiscuous earwig species,
Euborellia plebeja
, provides an empirical example of this type of indirect CFC. The elongated female sperm-storage organs
allow only partial removal and displacement of stored sperm by shorter male genitalia, resulting in a 20 % gain in paternity per mating. In staged mating trials, large males dominated male–male competition for burrows housing females, resulting in a significant increase in paternity by repeated matings with the same female. A numerical simulation based on this mating pattern showed that restricted sperm displacement
(~20 % per mating) is optimal for females to accumulate sperm from larger males. Given that male body size is heritable, females were estimated to gain a 1.4 % increase in their sons’ mating success as a genetic benefit. Advantages and disadvantages of indirect CFC
are discussed and compared with precopulatory mate choice and direct CFC.
Theory predicts that costly secondary sexual traits will evolve heightened condition dependence, and many studies have reported strong condition dependence of signal and weapon traits in a variety of species. However, although genital structures often play key roles in intersexual interactions and appear to be subject to sexual or sexually antagonistic selection, few studies have examined the condition dependence of genital structures, especially in both sexes simultaneously. We investigated the responses of male and female genital structures to manipulation of larval diet quality (new versus once-used mung beans) in the bruchid seed beetle Callosobruchus maculatus. We quantified effects on mean relative size and static allometry of the male aedeagus, aedeagal spines, flap and paramere and the female reproductive tract and bursal spines. None of the male traits showed a significant effect of diet quality. In females, we found that longer bursal spines (relative to body size) were expressed on low-quality diet. Although the function of bursal spines is poorly understood, we suggest that greater bursal spine length in low-condition females may represent a sexually antagonistic adaptation. Overall, we found no evidence that genital traits in C. maculatus are expressed to a greater extent when nutrients are more abundant. This suggests that, even though some genital traits appear to function as secondary sexual traits, genital traits do not exhibit heightened condition dependence in this species. We discuss possible reasons for this finding.
© 2015 European Society For Evolutionary Biology. Journal of Evolutionary Biology © 2015 European Society For Evolutionary Biology.
Cryptic female choice
(CFC) in spiders may involve several mechanisms to bias paternity including early termination of copulation, remating likelihood, and sperm dumping
. In Pholcidae
, these mechanisms seem to be very common and will be examined in the present chapter. In the Pholcidae
Physocyclus globosus
, sperm dumping involves an active role of the female. In contrast, in the Pholcidae Holocnemus pluchei
, sperm mass ejection during copulation is mainly under male control. In another haplogyne spider, the Oonopidae
Opopaea fosuma
, females are able to influence male’s chances of rearing their offspring by also exerting CFC by sperm dumping. Among pholcids, rhythmic genitalic movements of the pedipalps
(squeezes
) during copulation have been interpreted as genitalic copulatory
courtship
. Additionally, recent studies have evaluated the possibility that the outcome of male–female copulatory communication affects paternity. Future attention to the behavior of both female and male, and to the possible dialogues during copulation, promises to be a valuable tool in understanding sexual interactions in these spiders.
Sperm storage, the extended maintenance of viable sperm, probably occurs in most internally fertilizing animals. Because it temporally separates mating from conception, sperm storage can be adaptive in ecologically diverse habitats and affect life histories, mating systems, cryptic female choice, sperm competition, and sexual conflict. Sperm storage can result from different selective forces acting on females and/or males, sometimes resulting in coevolution. The various criteria often used to determine the presence of sperm storage in any given taxon can result from the action of any one or all of these selective forces. Here we discuss the criteria used to study sperm storage and how we can use these to better understand the evolution of diversity in sperm-storage adaptations.
Copyright © 2015 Elsevier Ltd. All rights reserved.
The entire process of the mating of the dragonfly Cordulia aenea amurensis Selys was observed at a pond (Horai-numa) near Sapporo, Hokkaido, in 1976. Some additional observations were also made in 1975 and 1983. Intra-male sperm translocation does not occur when males are in tandem with females but is executed when they are taking part in nonsexual activities (e.g. patrolling). The behavior of both sexes while they are copulating is described in detail. The duration of copulation takes from 37 to 62 min., during which a characteristic rhythmical movement of the anterior segments of the male abdomen is observed. The ultimate factors in the behavioral traits that occur during mating, such as the undulation of the male abdomen, along copulation time and departure from the pond while copulating are discussed from the view point of reproductive success, especially of sperm competition.
One hundred years after Darwin considered how sexual selection shapes the behavioral and morphological characteristics of males for acquiring mates, Parker realized that sexual selection continues after mating through sperm competition. Because females often mate with multiple males before producing offspring, selection favors adaptations that allow males to preempt sperm from previous males and to prevent their own sperm from preemption by future males. Since the 1970s, this area of research has seen exponential growth, and biologists now recognize sperm competition as an evolutionary force that drives such adaptations as mate guarding, genital morphology, and ejaculate chemistry across all animal taxa. The insects have been critical to this research, and they still offer the greatest potential to reveal fully the evolutionary consequences of sperm competition.
This book analyzes and extends thirty years of theoretical and empirical work on insect sperm competition. It considers both male and female interests in sperm utilization and the sexual conflict that can arise when these differ. It covers the mechanics of sperm transfer and utilization, morphology, physiology, and behavior. Sperm competition is shown to have dramatic effects on adaptation in the context of reproduction as well as far-reaching ramifications on life-history evolution and speciation.
Rapid divergent evolution of male genitalia is one of the most general
evolutionary trends in animals with internal fertilization; the shapes
of genital traits often provide the only reliable characters for species
identification. Yet the evolutionary processes responsible for this
pattern remain obscure. The long-standing lock-and-key hypothesis, still
popular among taxonomists, suggests that genitalia evolve by
pre-insemination hybridization avoidance; that is, hybrid inferiority
drives the evolution of male genitalia with a proper mechanical fit to
female genitalia. The sexual selection hypothesis,, in contrast,
proposes that divergent evolution of genitalia is the result of sexual
selection, brought about by variation in postinsemination paternity
success among males. Here, by comparing pairs of related clades of
insects that differ in mating system, I assess how the opportunity for
postmating sexual selection affects the rate of divergent evolution of
male genitalia. Genital evolution is more than twice as divergent in
groups in which females mate several times than in groups in which
females mate only once. This pattern is not found for other
morphological traits. These findings provide strong empirical evidence
in favour of a postmating sexual selection mechanism of genital
evolution.
Males of the damselfly Mnais pruinosa pruinosa were observed to use three different tactics to secure mates. The mean duration of copulation differed between the three observed tatics and re-sulted in varying degrees of sperm removal and insemination. It is shown that the last male to mate had almost 100% sperm precedence immediately after copulation regardless of the duration of copu-lation and therefore the quantity of sperm re-moved. In situations where less than 100% of ri-vals' sperm was removed the sperm from different males mixed within the female sperm storage or-gans over a period of about 6 days: sperm mixing produced variation in last male sperm precedence. The significance of sperm mixing in M. p. pruinosa is discussed in the context of the observed mate-securing tactics and the frequent female habit (37% of observations) of ovipositing without re-mating during an oviposition bout.
This paper is dedicated to Philip S. Corbet on the occasion of his 70th birthday.AbstractA small population of Ischnura pumilio in NW Spain was studied by marking and resighting in August-September 1996. A total of 142 males and 100 females were captured. Adults of I. pumilio appeared in two clear groups, starting on 31 August and 10 September. Population size was estimated about 1-2 individuals from 14 to 30 August but suddenly increased to 30-50 males and 40-120 females from 31 August to 13 September. A large fraction of males (43.6%) were never seen to mate, but only 13 females were never seen in copula. Androchrome females were rare (14 females) and did not differ from gynochrome females in fitness correlates. Copulation duration ranged from 1 to 5 h, and was dependent on time of day. The analysis of survival and recapture rates indicates that males and females have similar survivorship, but sex had a significant effect on recapture probability.
Copulation in the damselfly Ischnura graellsii lasted 1–5 h, and took place in the afternoon and evening at the study site in north-west Spain. Copula duration was measured in the laboratory under controlled temperature, humidity, photoperiod and density. At high density (15–20 males/insectary), copulations that started early in the day were always long, while at low density (two males/insectary) they could be short or long. At both densities, copulations with previously mated females were longer than with unmated females. The duration of stage II of copulation, when the male transfers sperm to the female, was constant and independent of density and time of day. A study of egg production in females mated only once indicated that copula duration is not correlated with the proportion of fertile eggs laid, and that females start running out of sperm after about 15 days. These results indicate that prolonged copulations of I. graellsii have a guarding function, but the existence of more sperm displacement in long copulations cannot be rejected. Guarding takes place during stage I of copulation, before the males invest sperm in the female, which is unusual. The relation between copula duration and postcopulatory behaviour in Ischnura species so far studied is discussed.
Insects and arachnids display the most impressive diversity of mating and social behaviour among all animals. This book investigates sexual competition in these groups, and the variety of ways in which males and females pursue, persuade, manipulate, control and help one another, enabling us to gain a better understanding of how conflicts and confluences of interest evolve together. Each chapter provides a comprehensive review of mating systems in particular insect and arachnid groups, discusses intrinsic and extrinsic factors responsible for observed mating strategies, and suggests fruitful avenues for further research. The book culminates in a synthesis, reviewing the date in terms of the theory of sexual conflict. This broad-based book will be of immense value to students and researchers interested in reproductive strategies, behavioural ecology, entomology and arachnology.
Traditionally, students of odonate reproductive behavior have focussed on how males compete for access to mates and fertilizations. This tendency has yielded considerable information on male reproductive strategies and on the proximate and ultimate mechanisms involved in male-male competition, but has left numerous gaps in our knowledge of other aspects of odonate mating systems. We review relevant aspects of odonate biology and examine the extent to which current data on mating patterns support predictions arising from sexual selection theory. Although long-term studies offer some such support , they also indicate that natural selection for longevity and stochastic factors such as weather play critical roles in influencing reproductive success. Relatively little of the variance in male reproductive success in odonates has been traced to variance in male phenotype. We emphasize the role of females as determinants of odonate mating patterns and discuss sexual conflicts of interest over mating, fertilization, and oviposition decisions. Finally, we explore ways in which natural selection underlies female mating decisions and how larval and adult ecology interact to influence adult reproductive behavior.
Male territorial behavior and female oviposition behavior of Megaloprepus coerulatus, a damselfly that develops in water-filled tree holes, is interpreted in light of its larval ecology. Sexual selection favors large males because they win more territorial contests than do smaller males, and females mate only in the vicinity of defended tree holes (i.e., passive female choice). Small males behave as territory holders until displaced, and/or act as subordinate satellites at large territories. Females are more predictably found in forest light gaps, even though they oviposit in both gap and understory tree holes. Males defended only 14% of the sites used by ovipositing females. Large tree holes are relatively rare, but support a greater number of emerging adults per season and produce larger adults than tree holes containing less-than-or-equal-to 1 L of water, which rarely produce more than one individual per season. By defending only large tree holes in gap areas, a male increases his chances of mating, and of producing multiple offspring and reproductively successful sons. Results from a field experiment suggest that both mate acquisition and procurement of superior larval habitats have been selective pressures in the evolution of male territory choice. Because even large holes are inadequate to support a female's entire clutch, and the presence of conspecific and heterospecific odonate larvae makes offspring survival uncertain, selection favors a female that partitions her clutch among multiple tree holes.
The reproductive behaviour of C. h. asturica is described. Males fought with each other for the possession of territories which contained the oviposition resource required by females. Females arrived at territories and either copulated and left the territory, copulated and oviposited in that territory or oviposited without a preceding copulation with the territorial male. Territorial males seemed to have a higher mating success than nonterritorial males. Males carried out courtship displays before and after copulation until females finished oviposition. Copulation was divided in two stages which were characterised by the nature of the male's abdominal flexions. The number of abdominal flexions during stage I and II was 50.2 ± 7.2 and 54.5 ± 16.7 (mean ± s.d.) respectively. The sexual behaviour of both sexes is discussed under current knowledge of sexual selection studies in Calopterygidae.
During copulation and before sperm transfer, odon. males are able to manipulate rival sperm stored in the female sperm storage organs (usually the bursa copulatrix. and spermathecae). males of the territorial C. h. asturica use 2 mechanisms for this. Bursal sperm is removed physically whilst spermathecal sperm is displaced via aedeagal stimulation (through a series of abdominal flexions) of the male sensory system that controls spermathecal sperm ejection. Most bursal sperm is removed but there is individual variation in spermathecal sperm displacement. Previous results have found that this variation is related to aedeagal width. In this paper 4 variables that may also explain variation in spermathecal sperm displacement ability are investigated., male age and status (territorial and nonterritorial), duration of the sperm displacement stage and the number of aedeagal stimulatory flexions. Variation in the ability to displace spermathecal sperm, however, was not related to these variables. This suggests that variation in this ability is reliant only on male genitalic attributes, aedeagal width. These results are briefly discussed in terms of current theory of sexual selection as the process propelling genitalic evolution.
The sexual behaviour and a case of male phenotypic dimorphism in P. quinta are described: black-winged (BW) males and hyaline-winged (HW) males. Similar to other territorial odon. spp., some males defended a space that females used for oviposition while other males acted as satellites. Copulation took place in 2 stages which differed in abdominal movement orientation and duration. Copulation duration varied between morphs and was frequently disrupted. During disruption, the genitalia of both sexes disengaged although the tandem position (the male's abdominal appendices grasping the female's prothorax) was maintained. Disruptions, which took place during the first stage (a stage during which displacement of rival sperm occurs in most odon. spp.), were sometimes followed by emissions of sperm from the vagina. Male morphs exhibit striking behavioural differences: HW males do not defend territories, but BW males do, and the former copulate for longer and show more copulatory disruptions. Some stages of female behaviour are described and suggested as instances during which females may be exerting mate choice: females copulated on fewer occasions with HW males, copulations with this morph were longer but ovipositions were not, and sperm emissions (possibly, sperm from previous mates) and copulatory disruptions of BW males were less frequent. Because of these differences, it is suggested this is a unique sp. to test current ideas of female control in an insect order in which the idea of male "control" has been traditional.
There is currently a gap in sexual selection theory about how much the environment drives female mating decisions. We present field data that suggest that female sexual behaviour in the damselfly Calopteryx haemorrhoidalis is influenced by parasite burden. Male wing pigmentation in Calopteryx is a sexually selected trait that signals a male's ability to cope with eugregarine parasites (an intestinal parasite that feeds on the adult's ingested food). Because adult C.haemorrhoidalis females also show wing pigmentation, we examined whether this trait is similarly influenced by parasite burden and whether it may signal the female's reproductive value. MaleC.haemorrhoidalis defend riverine substrates that females use for oviposition. After copulation and during oviposition, females are guarded by the copulating male against intruder males. Alternatively, females may avoid mating and ‘steal’ an oviposition site within a male's territory. In the present study, we found that the amount of female wing pigmentation was negatively correlated with the number of eugregarines present. Females with more parasites produced fewer eggs, survived fewer days, spent less time during courtship, ‘inspected’ fewer males before mating, had a lower mating success, were guarded for less time during oviposition and engaged in fewer ‘stealing’ events during oviposition. The reduced egg production and survival of heavily infected females may result from eugregarine depletion of the females' consumed food reserves. Thus, to offset reduced longevity, heavily infected females may accept a mating more rapidly and mate with fewer males. ‘Stealing’ behaviour may be related to the female's differential use of sperm from some males, particularly high-quality males. Interestingly, males that mated with low-pigmented females showed greater variance in wing pigmentation than did males that mated with high-pigmented females. Possibly, female wing pigmentation may signal a female's reproductive value, which provides females with longer mate-guarding episodes and reduced interference from intruder males. This study points out one possible constraint, intestine parasites, that females may face during mating decisions. Because females in bad condition mate with males in both good and bad condition, this constraint may be pervasive enough to weaken the intensity of selection for a male sexually selected trait, wing pigmentation, and help to maintain its variation in phenotypic expression. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.
The genitalia have a "design" remarkably similar to those of other representatives of the family. The main ♀ structure are the bursa coupulatrix, a T-shaped spermatheca, a pair of vaginal plates bearing a variable number of mechanoreceptive sensilla, and a ganglion located at the VIII abdominal segment. The ♂ intromittent organ is a curved, sclerotised aedeagus that ends in a distal penis head. This latter structure bears 2 lateral appendages which are covered by recurved spines. A construction of the fertilisation and copulatory events is proposed based on descriptive and experimental evidence in other zygopterans as well as in this pecies. The female genital anatomy suggests fertilisation occurs in the manner proposed for other odonates. Experimental evidence shown in this work suggests that, during fertilisation, the egg stimulates the mechanoreceptive sensilla and elicits contractile activity of the muscles that surround the sperm storage organs (SSOs). The contractile activity is likely to be mediated by the VIII abdominal segment ganglion. As a consequence of the muscular contractions, the SSOs ejects sperm which arrive to the site where the egg is and fertilise it. During copulation, the aedeagus "imitates" the presence of an egg in the vaginal plates and stimulates the mechanoreceptive sensilla inducing spermathecal sperm ejection. It is likely that spermathecal sperm is ejected to the bursa copulatrix where it is removed by the penis head and lateral appendages. After this sperm displacement process, the copulating males's sperm, stored in the seminal vesicle, is transferred, through a canal-like passage, by the aedeagus to the SSOs ♀ ♀ exhibit a considerable intra- and inter-individual variation in sensillum distribution and number on the plates, it is discussed whether this may have an adaptive significance in terms of retaining more control over stored sperm for ♀ ♀ during ♂ stimulation.
Insects and arachnids display the most impressive diversity of mating and social behaviour among all animals. This book investigates sexual competition in these groups, and the variety of ways in which males and females pursue, persuade, manipulate, control and help one another, enabling us to gain a better understanding of how conflicts and confluences of interest evolve together. Each chapter provides a comprehensive review of mating systems in particular insect and arachnid groups, discusses intrinsic and extrinsic factors responsible for observed mating strategies, and suggests fruitful avenues for further research. The book culminates in a synthesis, reviewing the date in terms of the theory of sexual conflict. This broad-based book will be of immense value to students and researchers interested in reproductive strategies, behavioural ecology, entomology and arachnology.
Male genitalia of 25 spp. are studied using scanning electron microscopy, and the structure of the fourth penile segment is described. Remarkable diversity exists among spp., particularly in the size and shape of the lateral lobes, and the morphology of the cornua. There are also differences in the number of cornua among the taxa surveyed. The surface of the lobes of many spp. is covered with spines which anchor the penis during copulation, and may trap and remove sperm when the penis is collapsed and withdrawn following copulation. Spp. are categorized according to the morphology of the penis and inferred patterns of sperm removal. Type 1 taxa possess relatively large, broad, flat lateral lobes, and lack cornua. or possess cornua that are greatly reduced in size. These spp, are believed to displace sperm in the bursa copulatrix before depositing their own sperm, thereby gaining positional priority during oviposition. Type 2 spp. possess elongated lateral lobes and/or cornua. These taxa are believed to engage in a mixed strategy of sperm displacement and sperm removal. Optimization of these characters on a phylogeny of the 3 genera indicates that the Type 1 sperm displacement strategy is ancestral, and that the Type 2 strategy was subsequently derived within the majority of the Libellula s.s. taxa.
To understand the relationship between copulation duration and sperm precedence in I. senegalensis, which mate for several hours, laboratory experiments and field observation were conducted. By irradiated male techniques, P2 value (sperm precedence of the last male to mate) was measured. P2 value was almost 100 % until 2 days after copulations regardless of the copulation duration. The interval between copulations in a female was about 2.3 days in the field. It is suggested that the last male to mate gains advantages in sperm precedence regardless of the copulation duration in the field. And complete sperm mixing (the point when the P2 value was 50 %) occurred 6 days after copulation.
The post-ovarian genital complex of Ischnura aurora aurora (Brauer) is situated on the eighth abdominal sternum just beneath the terminal abdominal ganglion. It is ectodermal in origin and consists of a bursa copulatrix. Spermatheca and vagina. The spermatheca opens into the bursa copulatrix through a long narrow spermathecal duct. The bursa copulatrix opens mid-dorsally into the vagina through a bursa communis which contains cuticular denticles. The cuticular intima of the vagina forms the anterior cuticular valves and the lateral plates. The posterior region of the vagina modifies into a genital atrium. The vagina is externally enveloped by three pairs of sternal muscles. The paired tubular female accessory sex glands with long ducts are lodged in the ninth abdominal segment and open into the genital atrium. The histological and scanning electron mcroscopic studies on POGC reveal various structural modifications in relation to sperm-storage, transport and fertilization of the egg in I.a. aurora.
Zygopterans belonging to the genusIschnuraare unusual amongst damselflies because of the variety of mate guarding techniques employed by males of different species. The lack of post-copulatory guarding combined with lengthy copulations in one group of ischnuran species suggest that these males guard femalesin copula. An examination of the accessory penes of species in this group indicates that all but one species have considerable microspination on the distal end (the flagella) of their penes that can function in sperm displacement. The flagella of these species are long and thin compared to those of other ischnurans. This is likely an adaptation to gain access to the spermatheca of the female. Two species tandem guard their mates during ovipositing. These species are the only ischnurans missing a stout pair of basal spines on the penultimate segments of their penes. They have considerable microspination over much of their penes but their flagella are of only moderate length and stout. Ischnurans that do not mate guard have short, stout flagella and most species examined from this group (5 of 7) have little microspination on their flagella tips. It is proposed that females of these species mate only once and therefore their males do not displace sperm.
Behavioural ecology is currently undergoing a paradigm shift, with the traditional concepts of the choosy, monogamous female and the coadapted gene complex increasingly giving way to the realization that sexual reproduction engenders conflicts, promotes polyandry, and thereby provides females with a cryptic arsenal of postcopulatory processes with which to safeguard their investment in large, costly eggs. As research focuses on reproduction from the female perspective, evidence is emerging that polyandry can provide genetic benefits that enhance female reproductive success. In this review, we propose that reproductive mode is a critically important factor influencing the type of genetic benefits that females gain by mating with more than one male. Among the hypotheses that propose genetic benefits to polyandry, there is a distinction between those that posit benefits from intrinsic (additive) effects of paternal genes in offspring, and those that propose a benefit resulting from defence against incompatibility. Polyandry to acquire superior paternal genes and polyandry as a defence against incompatibility are not mutually exclusive hypotheses. However, evidence from reproductive physiology, immunology and evolutionary conflict theory suggest that development of the embryo within the female makes polyandry for incompatibility avoidance far more important for viviparous females than for females that lay eggs.
The objective of this study is to describe the copulatory and ovipositional behaviour of
Hetaerina americana
and
H. titia
, and to depict any differences in such behaviour as may exist between these two species. It is quite important in such studies to understand the mechanisms which assure conspecific mating. Both
americana
and
titia
are found breeding together on many of the streams of central Texas. Williamson (1906) pointed out that species in which the abdominal appendages were very similar often had sexually dimorphic and/or specifically distinct wing coloration, while species with clear wings had quite distinct abdominal appendages. These different wing patterns were suggested as functioning in species recognition for conspecific mating. Buchholtz (1951, 1955) experimentally verified that the females of
Calopteryx splendens
recognize and respond to males of their own species through a set of optical stimuli including the color pattern of the wing. Loibl (1958) and Krieger and Krieger-Lobl (1958) experimentally demonstrated that in
Lestes dryas, L. sponsa, Ischnura elegans
and
I. pumila
, all of which have clear, colorless wings, the species recognition factors are the shape of the abdominal appendages and body coloration. Williamson's early inferences appear to have been well documented.
Before mating, all male odonates translocate sperm from the testes (IX segment) to the penis (II segment), but inCoenagrion scitulumthis behaviour is repeated up to six times during copulation. The aim of this study was to find an explanation for this unusual behaviour. Copulation behaviour consists of three to seven cycles, each of which includes one intra-male sperm translocation, one stage I and one stage II (i.e. the complete copulatory sequence typical of zygopterans). The duration of pre-copulatory tandem and cycle 1 of copulation was negatively correlated with time of day and positively with male disturbance. Males captured during stage I of any copulatory cycle always had the seminal vesicle full of sperm, thus indicating that they do translocate sperm during sperm translocation behaviour. Females were inseminated at stage II. The volume of ejaculate in females in the field interrupted during stage I of the first copulatory cycle was not significantly different from the volume stored by pre-copula females indicating that males cannot remove a significant amount of sperm from the female's genital tract at this stage. Spines on the horns of the penis, which in other damselflies help remove the sperm stored by females, are, however, absent inC.scitulum. Experiments with virgin females that received up to five inseminations indicated that the sperm are progressively packed, and therefore the volume is not directly proportional to the number of inseminations. MaleC.scitulumthus has a poor sperm removal ability and multiple intra-male sperm translocation and insemination of the female during the same copulatory act seems to be a mechanism of sperm competition by which the male achieves a greater fertilization success.
By removing males and controlling the rate of water flow past oviposition patches in an experimental area, we showed that female Calopteryx splendens xanthostoma preferred to oviposit in fast flowing water rather than slow flowing water. A series of manipulations revealed the fitness benefits to females for this preference: eggs placed in fast-flowing water developed significantly faster and showed significantly lower mortality than eggs placed in slow-flowing water. A major factor determining this difference was the deposition and growth of encrusting algae which prevented the successful hatching of eggs in slow-flowing water.
Rearing damselflies under laboratory conditions is a promising means of solving a variety of biological questions. Therefore, in order to improve the success of future researchers we felt the need to indicate potential difficulties in carrying out rearing experiments. Laboratory crosses were obtained using virgin animals originating from natural populations in Belgium and Spain. Resulting offspring was maintained, under laboratory conditions, in small aquaria until emergence and in insectaries as adults. Our results show that keeping damselflies during their entire life cycle under artificial conditions can be very difficult. We suggest that future researchers should change water regularly, supply sufficient food, and rear animals at low density or even individually. Furthermore, suggestions are given on type of food, advisable laboratory conditions and female oviposition methodology.
Female Calopteryx splendens xanthostoma have discrete sperm storage
organs and secure oviposition in one of two ways: a female either mates
with a male who subsequently guards her whilst she oviposits (MAG), or
females can secure access to an oviposition site without copulating with
the resident male (SAG). Random amplified polymorphic DNA (RAPD)
analysis of the genetic diversity of sperm from individual sperm storage
organs revealed that the spermathecae contained sperm of a greater
genetic diversity than sperm in the bursa copulatrix. Males cannot
remove sperm from the spermathecae during copulation, and we propose
that the spermathecae might function as a sperm cache for the sperm of
previous mates. Females that conduct SAG ovipositions have a higher
genetic diversity of stored sperm than MAG females. We suggest that
females which gain access to oviposition sites without remating have the
potential to exercise postcopulatory choice during oviposition, on the
basis of: (i) the observed patterns of sperm precedence in other
calopterygids; (ii) the variation in genetic diversity of stored sperm;
and (iii) the avoidance of recopulation in SAG females.
