Genital Evolution: the Traumas of Sex first with One Palp and Then with the Other

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Genital Evolution: The Traumas of Sex first with one palp and then with the other. While sounding rather brutal, this does the trick and Copulating males usually insert their penis into the female and ejaculate in her females produce fertilized eggs reproductive tract; but in some species, males are more invasive, puncturing sometime later. It has been the female body-wall and inseminating directly into her body-cavity. A spider suggested that the hypodermic has just been added to this list and new perspectives provided on why males pedi-palp evolved in response to harm females during copulation in the first place. sperm competition [7] and although there has been some correlated D.J. Hosken and T.A.R. Price to cut-to-the-chase and get sperm evolution in females — namely directly to the eggs. Traumatic atrophy of the ‘normal’ reproductive The male genitalia of internal fertilizers insemination appears to be one tract — there has been no evolution are among the fastest evolving fantastic way to achieve this end, of any device to ameliorate potential characters, and even in species with and a spider has just been added to costs of male stabbing. In this no other obvious morphological the list of animals employing this regard, the spiders differ from bed differences, the penis is usually behaviour [5]. bugs where females in some distinctive enough to allow species Traumatic insemination occurs species have evolved structures differentiation [1]. Male genitalia are when, rather than introducing sperm that appear to reduce costs of also frequently elaborated to the point into the female reproductive tract, traumatic insemination [5]. This of lunacy (Figure 1), which belies their males instead penetrate the female has been taken to extremes in simple function, to transfer sperm from body wall and inject sperm into the some groups, where in essence, male to female. Sexual selection is now body cavity. The most impressive a new female reproductive tract widely accepted to be responsible for examples of traumatic insemination has evolved [5]. penis (and associated structure) occur when penetration is through Sexual nastiness is well evolution, and one component of the external body wall — rather than documented, with females in some sexual selection, sperm competition, is through the vaginal wall — and the species, famously praying mantises, thought to be pivotal in the evolutionary best documented cases are in eating males during or after copulation. origins of the penis [2]. Rather than wait bed-bugs. Bed-bug males use The benefits of this are clear: good for a female to eject her eggs, a penis a modified structure (paramere) that nutrition, and once a female has allows sperm to be placed well inside resembles a hypodermic needle to a male’s sperm he is often of no further the female, providing these gametes penetrate the external wall of the use to her, hence the selective with a head-start in the race with rivals female abdomen and inseminate advantage of eating males [8]. But it is to fertilize ova. But females have not there [6], and similar types of more difficult to understand why males been mere sperm-receptacles in the traumatic insemination have been physically damage females during competition between males, and their reported for several other insect copulation, because at first sight it reproductive tracts are veritable species [7]. Now traumatic makes little sense to harm the female obstacle courses that are often insemination has been described in that is going to produce your offspring: extremely hostile environments in a spider, the aptly named Harpactea after all, she might die before which sperm must survive [3,4]. The sadistica [5], and although spiders reproducing. Furthermore, physical complexity of the female reproductive use a modified mouth-part damage to females during copulation tract has probably evolved to provide (pedi-palp), rather than a true penis, is not just limited to species with females with some control over to inseminate females, the form of traumatic insemination, being well fertilization [4], and typically sperm do the stabbing component of the documented in other insects [9,10]. not have direct access to ova, but must pedi-palp is very similar to the Several adaptive hypotheses have wait in specialised structures or bed-bug needle. During mating, been proposed to explain this protected sites for the female to release male H. sadistica grab females and phenomenon [11]. Perhaps males are unfertilized eggs. One way a male could then bite them, which usually causes trying to make mating so unpalatable regain a fertilization advantage over the female to become motionless. that females will never remate, and rivals and circumvent female Then, after some manoeuvering, the hence damaging males will secure all fertilization interests, which may not male inseminates the female by subsequent female reproductive coincide with the male’s, would be repeatedly stabbing her abdomen output. Alternatively, perhaps males Current Biology Vol 19 No 13 R520

context — sperm competition — has inadvertently resulted in males harming females [14], a situation that is also found in Drosophila melanogaster where males with ejaculates that are most toxic to females are the best at sperm competition [16]. These are both instances of post-copulatory male–male competition being detrimental to females, and clearly highlight a reason for males harming females during copulation. We have been aware that precopulatory male–male competition can also result in female damage or death for some time, with well documented examples in elephant seals and yellow dung flies [17,18]. Unfortunately for females, this machismo does not end at copulation as the beetle data show, and researchers working on other taxa with copulatory harm should also pursue the male–male competition and collateral damage avenue. Returning to the spiders, while we do not know if the repeated stabbing females suffer during copulation is costly for them — apparently they do not bleed for example — what is clear, and made clearer by the spider description, is that the structures used in external-traumatic insemination are often very simple. The spider pedi-palps and the bed-bugs parameres clearly have very different developmental and evolutionary origins. Nevertheless, they look very similar. In contrast, genitals that enter the female reproductive tract, even if they cause damage, and even if they are used in internal-traumatic insemination, are much more complicated structures [6]. This pattern has some bearing on our Figure 1. An example of the sorts of genital elaboration seen across internal fertilizing animals. understanding of genital evolution Shown here are parts of the male genitalia of several dungfly species. (A) Cordilura pubera; (B) more generally. It has been argued that Scathophaga cineraria; (C) Norellia spinimana; (D) Cordilura ciliata. Images courtesy of Aria male–female conflict is fundamentally Minder. important in penis evolution, and that this conflict explains the rapid, crazy are trying to trick females into females are also superior sperm divergence of penis form [19]. If so, investing more in current reproduction competitors, so that male–male taxa where males circumvent the by reducing the likelihood they will competition is again at the root of normal fertilization route and break the survive for later attempts — or at female woes. In these beetles it had main barrier to infection — the body least making females think so. previously been shown that the spiky integumen — by stabbing females to Basically, inducing a terminal penis damages the female during transfer sperm should be groups with investment response. copulation [9]. Additionally, females substantial realised sexual conflict Unfortunately, there is little empirical of beetle species with a spinier penis focussed on the organ of sperm support for either of these ideas [12,13], had thicker walls in their reproductive transfer. As noted above, however, and so perhaps damage is merely tracts, presumably an evolved these structures are amongst the most collateral. But if so, collateral to what? response to prevent greater damage simple and convergent of organs used Recent work on the seed beetle [15]. But none of the adaptive harm in internal fertilization. Callosobruchus maculatus provides hypotheses seemed to apply to Perhaps there really is only one way one answer [14]. This study found that male damage in this group [13].We to produce a hypodermic needle [6], but males that are more damaging to now know why. 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Second Messenger Signaling: concentrate on TPC2. The rationale for analyzing whether TPC2 might be Multiple Receptors for NAADP activated by NAADP came from studies revealing its lysosomal localization [4]. Previously Churchill and colleagues [5] The second messenger NAADP appears to have an essential role as a universal identified the reserve granule of sea trigger of Ca2+ signaling. Following on from previously published NAADP urchin eggs — a similar organelle to the receptor candidates, recent work now describes the identification of a novel lysosome — as the intracellular target NAADP-sensitive Ca2+ channel. organelle for NAADP. Intracellular localization of TPC2 to lysosomes Andreas H. Guse 2002 by Hohenegger and colleagues and the similarity of TPC2 to Ca2+ [2]. A second candidate followed channels prompted Calcraft et al. [4] Ca2+ signaling is one of the in 2007, when Zhang et al. [3] to carry out NAADP-binding studies fundamental intracellular signaling introduced transient receptor potential with membranes from wild-type or systems that transduces extracellular mucolipin 1 channel (TRP-ML1) as an TPC2-expressing HEK cells. Specific information into cellular responses. NAADP-sensitive Ca2+ channel. NAADP binding was increased Ca2+-mobilizing second messengers Now Calcraft et al. [4] describe the threefold in TPC2-expressing play a pivotal role in this process. identification of a new class of NAADP cells and this increase could be Among these, nicotinic acid adenine receptors, the two-pore channels abolished by immunoprecipitation dinucleotide phosphate (NAADP) (TPCs). In this work the authors of TPC2 [4]. Ligand competition appears to act as a universal trigger demonstrate NAADP-mediated revealed two distinct binding sites of Ca2+ signaling (reviewed in [1]). activation of TPC2, one of the TPC with nanomolar and micromolar The receptor for NAADP has been family members, when expressed in affinities. a matter of debate since the first HEK293 cells. Although some data Uncaging of NAADP in candidate — the type 1 ryanodine deal with other TPC family members, TPC2-expressing HEK cells resulted receptor (RyR1) — was presented in e.g. TPC1 and TPC3, the authors in biphasic Ca2+ signaling, whereas