Highly variable sperm precedence in the stalk-eyed fly, Teleopsis dalmanni

BMC Evolutionary Biology Highly variable sperm precedence in the stalk-eyed fly, Teleopsis dalmanni Laura S Corley 1 2 Samuel Cotton 2 Ellen McConnell 2 Tracey Chapman 0 Kevin Fowler 2 Andrew Pomiankowski 2 0 Department of Biology, University College London , Darwin Building, Gower Street, London, WC1E 6BT , UK 1 Department of Entomology, Washington State University , Pullman WA 99164-6382 , USA 2 Galton Laboratory, Department of Biology, University College London , Wolfson House, 4 Stephenson Way, London NW1 2HE , UK Background: When females mate with different males, competition for fertilizations occurs after insemination. Such sperm competition is usually summarized at the level of the population or species by the parameter, P2, defined as the proportion of offspring sired by the second male in double mating trials. However, considerable variation in P2 may occur within populations, and such variation limits the utility of population-wide or species P2 estimates as descriptors of sperm usage. To fully understand the causes and consequences of sperm competition requires estimates of not only mean P2, but also intra-specific variation in P2. Here we investigate within-population quantitative variation in P2 using a controlled mating experiment and microsatellite profiling of progeny in the multiply mating stalk-eyed fly, Teleopsis dalmanni. Results: We genotyped 381 offspring from 22 dam-sire pair families at four microsatellite loci. The mean population-wide P2 value of 0.40 was not significantly different from that expected under random sperm mixing (i.e. P2 = 0.5). However, patterns of paternity were highly variable between individual families; almost half of families displayed extreme second male biases resulting in zero or complete paternity, whereas only about one third of families had P2 values of 0.5, the remainder had significant, but moderate, paternity skew. Conclusion: Our data suggest that all modes of ejaculate competition, from extreme sperm precedence to complete sperm mixing, occur in T. dalmanni. Thus the population mean P2 value does not reflect the high underlying variance in familial P2. We discuss some of the potential causes and consequences of post-copulatory sexual selection in this important model species. - Background When females copulate with more than one partner, competition for fertilizations occurs after insemination. Such post-copulatory sexual selection can be a potent evolutionary force, as is evidenced by the numerous male behavioral, physiological, and morphological adaptations that influence sperm competition, such as mate guarding, increased copulation duration, seminal fluid induced reluctance of female re-mating, and the mechanical removal of sperm [1-3]. In addition, post-copulatory sexual selection can enhance or diminish male ornament evolution if ornament size covaries positively or negatively, respectively, with sperm competitive ability [4-6]. The most widely used metric for sperm competition that is used to infer patterns of paternity is the proportion of eggs sired by the second male in controlled double-mating trials (P2; [7]). Species or population level studies of P2 have been used extensively to describe sperm competition, particularly in insects [2] and birds [1]. However, considerable variation in P2 often occurs between populations and individuals, and intra-specific values of P2 can range from zero to one [2,5,8]. Such variation can severely limit the utility of population-wide (or species) P2 estimates as descriptors of sperm usage, because it fails to account for variation in male performance (P2 is derived from the performance of both first and second males), or aspects of female morphology and behaviour, such as sperm storage, that may differ between individual females [9]. For example, within many Lepidopteran species, some females lay eggs fertilized almost exclusively by the first male to mate, whereas others show strong second male sperm precedence ([10]; see also [11] for an example in guppies); in these instances mean P2 values do not reflect the underlying bimodal distribution of male fertilization success. So in order to fully understand the causes and consequences of sperm competition it is necessary to estimate not only mean levels of sperm precedence, but also intra-specific variation around that mean. Numerous factors have been shown to influence intraspecific variation in P2 including male size, sexual ornamentation, mating history, reproductive organ size and diet [2,3,5]. There is also support for the hypothesis that males tailor their ejaculate in response to female factors such as size, mating status, age, fecundity and familiarity [12]. In addition, evidence is accumulating that, contrary to traditional views, ejaculates are in fact costly and cannot be produced in limitless quantities [12,13], and that male gamete availability can limit zygote formation. Under sperm-limitation, reproductive asymmetry between the sexes for variance in fertilisation success, and with it the advantage of sperm competition for available ova, will be reduced. Nonetheless, if a particular mating role is favoured (e.g. first rather than last), a male is still predicted to invest more in the favoured role [14]. Spermlimitation phenotypes are most commonly seen in freespawning external fertilizers at low density [15-17], although similar selective environments may be common in internal fertilisers when females receive insufficient sperm to fertilise all of their eggs [e.g. [12,18]]. Stalk-eyed flies (Diptera:Diopsidae) are increasingly important model organisms for studies of sexual selection [19-22]. They are characterised by the lateral extension of the eyes on elongate protuberances on the side of the head capsule, a trait common to both sexes in all species [19,23]. In many species the eyespan of males is greater than that of females, the result of sexual selection through female mate choice [24-29] and male-male competition [30,31]. The Malaysian stalk-eyed fly, Teleopsis dalmanni (formerly known as Cyrtodiopsis dalmanni; [32]), exhibits extreme sexual dimorphism for eyespan resulting from strong intra- and inter-sexual selection on the trait in males (ibid.). Females form large harems on root hairs overhanging the eroded banks of streams and males compete to control these harems [19,33]. Both sexes are highly promiscuous and mate at high frequencies (~10 and 6 times per hour in the laboratory, for males and females respectively; [34,35]). There is also some evidence that males strategically allocate more ejaculate to larger, more productive females through the production and delivery of larger spermatophores [36]. However, T. dalmanni spermatophores are small [37] and females store few sperm following a single mating (~140; [36]). Females are therefore sperm-limited and must copulate repeatedly to attain maximal fertility [38]. This problem is exacerbated in large, highly fecund females despite b (...truncated)