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Title: A biological switching valve evolved in the female of a sex-role reversed cave insect to receive multiple seminal packages}
Article:
Abstract:
We report a functional switching valve within the female genitalia of the Brazilian cave insect Neotrogla. The valve complex is composed of two plate-like sclerites, a closure element, and in-and-outflow canals. Females have a penis-like intromittent organ to coercively anchor males and obtain voluminous semen. The semen is packed in a capsule, whose formation is initiated by seminal injection. It is not only used for fertilization but also consumed by the female as nutrition. The valve complex has two slots for insemination so that Neotrogla can continue mating while the first slot is occupied. In conjunction with the female penis, this switching valve is a morphological novelty enabling females to compete for seminal gifts in their nutrient-poor cave habitats through long copulation times and multiple seminal injections. The evolution of this switching valve may have been a prerequisite for the reversal of the intromittent organ in Neotrogla.
Introduction:
Many man-made engineering solutions have evolved already in insects. Such examples include hinges( flapping flight enabled by the wing base: Brodsky, 1994), on-off valves( spiracle openings to regulate airflow: Chapman, 1998), backflow valves( the bombardier beetle's defensive spray: Arndt et al., 2015), coiling mechanisms( genital tubes: Matsumura et al., 2017a) or catapult-like mechanisms( the legs of many jumping insects: Burrows, 2013). Some mechanisms that were formerly thought to be unique to human engineering have been discovered recently in insects: biological screws have been found in a beetle's leg( van de Kamp et al., 2011), and interacting gears were found in the jumping legs of planthoppers( Burrows and Sutton, 2013). The design and construction of such mechanisms on a micrometer scale is a challenging task in engineering( Feinberg et al., 2001). Therefore, studies of micron-scale biological structures can be rewarding as they illuminate construction principles in insects that could be applied to technical solutions in engineering( Matsumura et al., 2017b). The genus Neotrogla( family Prionoglarididae) is a minute Brazilian cave insect belonging to the order Psocodea( booklice, barklice, and parasitic lice). This genus is of special evolutionary and morphological interest because of the reversal in its genital structures( Yoshizawa et al., 2014). The females of Neotrogla have a penis-like intromittent organ( gynosome: Figure 1A), which is inserted to a male vagina-like genital cavity for copulation. During mating, the male injects liquid semen into the female’s sperm storage organ( spermatheca) through the opening of the spermathcal duct at the tip of the female penis. Within the spermatheca, the injected semen then induces the formation of a hard capsule shell around itself( Figure 1A, B: Wearing-Wilde( 1995); Yoshizawa et al., 2014). Although there is only a single inlet spermathecal duct present, occasionally two seminal capsules are attached simultaneously to a plate-like structure on the spermatheca( termed ‘spermathecal plate’:[Lienhard et al., 1893; Yoshizawa et al., 2014]). The semen within the capsule is used not only for fertilization but is also consumed by the female as nutrition. To compete for nutritious semen, the direction of sexual selection is reversed in Neotrogla( sex-role reversal: Yoshizawa et al., 2014). Each seminal capsule is voluminous( ~0. 05 mm3, corresponding to ~300 ml scaled up to humans), and the duration of the copulation is very long( for 40 to 70 hr). In a closely related species lacking reversal of genital structure( Lepinotus patruelis, Trogiidae), the seminal transfer for forming a similarly voluminous seminal capsule is known to complete in 50 min( Wearing-Wilde, 1995). The female penis of Neotrogla bears a lot of spines, by which females anchor a male coercively during copulation. Therefore, females are obviously responsible for this very long copulation, probably to obtain more semen from a male( Yoshizawa et al., 2014). After consumption of the semen, the empty capsule is detached from the plate, which is kept within the spermatheca. Because females frequently have empty capsules within the spermathecal pouch( in an extreme case, up to nine empty capsules and two filled ones attached to the plate were observed: Yoshizawa et al., 2014), female Neotrogla can be considered polyandrous, which is apparently controlled actively by the female. Although several examples of sex-role reversed animals induced by seminal gifting have been reported, Neotrogla so far is the only example with a morphological reversal of its intromittent organs( Kamimura and Yoshizawa, 2017). This morphological reversal seems to require further upstream modifications of the genital system, such as the formation of the spermathecal plate, which was reported as an additional novelty tightly associated with the seminal gifting( Lienhard et al., 1893; Yoshizawa et al., 2014). However, the detailed morphology and function of this spermathecal plate, which presumably plays an important role in the evolution of the female penis, remained unclear due to the extremely small size of the involved subcomponents and their fragile spatial composition. In this study, we investigated the structure of the spermathecal plate by using a combination of confocal laser scanning microscopy( CLSM) and high-resolution synchrotron microcomputed tomography( HR-µCT) to assess the functional morphology of sperm storage and control of seminal flow. We examined three species of Neotrogla( N. brasiliensis, N. aurora and N. truncata), the spermathecal morphology of which is practically identical( Lienhard et al., 1893). Based on the results, we discuss the evolutionary significance of this plate during the evolution of the reversed intromittent organs in Neotrogla.
Discussion:
The present analyses show that females of Neotrogla use a special mechanism to actively control the direction of seminal flow( Figures 1E and 2A–D). This biological switching valve allows females to receive two seminal packages( i. e., more nutrition) from the same or different males within a short time span. In particular, the switching valve allows to receive a second seminal capsule while the first one is consumed. A similar but less sclerotized structure can be observed in close relatives of Neotrogla( Sensitibilla and Afrotrogla, all belonging to the tribe Sensitibillini), suggesting that the structure probably originated in their common ancestor( Lienhard, 1893; Lienhard et al., 1893). Neotrogla is distributed in South America, whereas Sensitibilla and Afrotrogla are distributed in southern Africa. Therefore, the origin of this switching valve dates to at least the break-up of the two continents, over 100 million years ago( Seton et al., 2012). In other psocodeans, no sclerite or muscle corresponding to those of the spermathecal plate elements have been observed( Badonnel, 1934; Klier, 1956; Wearing-Wilde, 1995). The spermathecal plate thus clearly represents an evolutionary novelty( Müller and Wagner, 2003). The mechanism of flow control and redirection within this biological switching valve is fundamentally different from that in man-made switching valves, which are used, for example in the oil and gas industry. Technical switching valves use the active rotation of tube or ball elements with various openings to redirect the flow and both closing as well as opening involve an active movement of the valve. In contrast, the observed biological switching valve involves a passive movement component. The seminal flow injected by a male is redirected by a differential inclination of the CE( Figure 2E). This inclination is due to the fan-like geometry of the actuator muscle whose parts can pull the CE in the preferred direction to work against the passive closing forces generated by the resilin patches around the valve complex. This muscle-closure element configuration could be advantageous since each muscle bundle pulls in an optimal direction to incline the CE into one of the two opening positions. Additionally, there is no need for lubrication since the moveable parts do not move against each other. Compared to technical switching valves, this design is advantageous to some extent because the muscle forces are not redirected via a lever arm. The presence of a spermathecal plate with a valve function to control seminal flow may further refine our understanding of the causes and consequences of the reversed sexual selection in this genus. Female-female competition for males( sex-role reversal) to receive nutritious seminal substances is considered as the most important factor driving the evolution of the female penis( Yoshizawa et al., 2014). Among all animals with known sex-role reversal, Neotrogla is the only example in which a female penis evolved( Kamimura and Yoshizawa, 2017). In a close relative of Neotrogla, the barklouse species Lepinotus patruelis( Wearing-Wilde, 1996), the sex-roles are also reversed, but the species possesses normal genital structures. Therefore, it is very likely that, in addition to the sex-role reversal, there is at least one other key factor that enabled the evolution of a female penis. Although females of all three known genera of Sensitibillini possess a spermathecal plate, females of Sensitibilla do not have a penis-like organ( Lienhard, 1893; Lienhard et al., 1893). This strongly suggests that the evolution of the spermathecal plate, possibly including a switching valve, preceded the evolution of the female penis. The spermathcal plate has two slots available for insemination( Figure 1E). In Neotrogla and the related species( Lepinotus), content of the capsule is digested as nutrition during the seminal capsule being attached to the spermathecal plate( the transparent capsule shown in Figure 1B is a digested and empty one: Yoshizawa et al., 2014). Therefore, if there is only one slot for insemination, as in the spermatheca of Lepinotus, females cannot receive another capsule while digesting one. With the switching valve, the female Neotrogla( and possibly Sensitibilla and Afrotrogla) can selectively use one of two slots for insemination, with leaving the other slot empty. This enables the females to immediately receive an additional seminal package from the same or other males by using the empty slot. Males are predicted to prudently allocate limited resources, such as nutritious seminal gifts and sperm, to multiple females, especially when operational sex ratio is biased to females, rendering female-female competition for male-derived nuptial gifts( i. e, propensity for multiple mating) more intense( Abe and Kamimura, 2015). The male-holding organ( spiny female penis) and female-induced long copulation durations of 40 – 70 hr( compared to just ~50 min for formation of one seminal capsule in close relatives) in Neotrogla( Yoshizawa et al., 2014) thus can be considered as exaggerated adaptations for such escalated competition for nuptial gifts in this group of insects inhabiting highly oligotrophic cave habitats( Lienhard and Ferreira, 2013; Lienhard and Ferreira, 2015; Yoshizawa et al., 2014). The condition of having two freshly deposited spermatophores at once is comparable to that in multiple sperm storage organs reported for females of some animal groups, such as dung flies, Drosophila, or tephritid fruit flies( Ward, 1993; Pitnick et al., 1999; Twig and Yuval, 2005). Although theory predicts that having multiple sperm stores can be a powerful mechanism for choosing sperm( Hellriegel and Ward, 1998), evidence is scarce for a gain in fitness by actively selecting for particular sperm from among multiple mates( e. g., Demont et al., 2012; Schäfer et al., 2013). In addition, in the case of Neotrogla and related barklice( Lepinotus patruelis), the content of the seminal capsule is digested quite rapidly if not used for fertilization( Wearing-Wilde, 1995; Yoshizawa et al., 2014). Therefore, the switching valve system reported here likely represents an adaptation for direct benefits( i. e., for obtaining more nutrients) rather than for genetic benefits( i. e., for choosing sperm from high-quality males).
In dry caves of southeastern Brazil , live a group of insects named Neotrogla that are perhaps best known because the egg-producing females have penises while the sperm-producing males have vaginas . The sex roles of these Brazilian cave insects are also reversed: females compete over the males , who in turn are selective of their female partners . This sex role reversal likely evolved within Neotrogla because the males’ semen represents a rich and reliable source of energy within a nutrient-poor cave environment . When females are not using semen to fertilize their eggs , they consume it . Yet , while other animals show sex role reversal , Neotrogla species alone have reversed sexual organs . Neotrogla penises are spiky and may have evolved so that females can anchor themselves to males and then mate for prolonged periods . This would allow the females to stock up on the nutritious semen . Compared to their closest relatives , Neotrogla species can hold twice as much semen within their sperm storage organs . Scientists have speculated that a valve-like structure within this organ enables this extra storage by allowing the female to redirect semen into two separate chambers . But the organ’s small size has made it difficult to determine its inner workings , and scientists have yet to discover a switching valve that serves such a purpose within the animal kingdom . Yoshizawa et al . examined three Neotrogla species using advanced imaging technology and detected the first example of a biological switching valve . Neotrogla females can control this valve , switching the flow of semen between two slots . In this way , females can store two batches of semen at once . Seemingly exploiting this adaptation , the females’ spiky penises help them restrain males until they have received multiple semen injections . Yoshizawa et al . therefore suggest the emergence of this valve within the sperm storage organ may have promoted the evolution of the female penis . Along with giving insight into the lives of cave insects , these findings are of interest to engineers , who face challenges when constructing valves on a microscopic scale . The unique switching valve of female Neotrogla may one day inspire new man-made machinery that could advance a range of industries .