Mechanisms Of Cryptic Female Choice Research Articles

Competitive Sperm-Marked Beetles for Monitoring Approaches in Genetic Biocontrol and Studies in Reproductive Biology.

Sperm marking provides a key tool for reproductive biology studies, but it also represents a valuable monitoring tool for genetic pest control strategies such as the sterile insect technique. Sperm-marked lines can be generated by introducing transgenes that mediate the expression of fluorescent proteins during spermatogenesis. The homozygous lines established by transgenesis approaches are going through a genetic bottleneck that can lead to reduced fitness. Transgenic SIT approaches have mostly focused on Dipteran and Lepidopteran pests so far. With this study, we provide sperm-marked lines for the Coleopteran pest model organism, the red flour beetle Tribolium castaneum, based on the β2-tubulin promoter/enhancer driving red (DsRed) or green (EGFP) fluorescence. The obtained lines are reasonably competitive and were thus used for our studies on reproductive biology, confirming the phenomenon of ‘last-male sperm precedence’ and that the spermathecae are deployed for long-term sperm storage, enabling the use of sperm from first mating events even after secondary mating events for a long period of time. The homozygosity and competitiveness of the lines will enable future studies to analyze the controlled process of sperm movement into the long-term storage organ as part of a post-mating cryptic female choice mechanism of this extremely promiscuous species.

Male performance and associated costs in successive sexual encounters in a polygynous web wolf spider

Polygynous males increase their reproductive success by fertilizing as many females as possible. However, this strategy can lead to costs for the males. This study focused on an atypical wolf spider that lives in webs, Aglaoctenus lagotis. Previous studies report polyandrous females, but little is known about the mating strategy of males and its potential associated costs. Our goals were to determine the potential polygyny and the changes in sexual behaviour, body condition and physiology of males throughout successive matings. Males were expected to mate with multiple females; males’ body condition was expected to decrease and male mating performance, including sperm transfer, was expected to decrease over successive matings. Males were exposed to successive virgin females every 3 days until the male did not court, was cannibalized or died of natural causes. Agreeing with our predictions, males were capable of multiple matings, showing an average of 5 ± 2 matings (range 3–11). Their mating performance decreased in successive matings and, although no changes were found in the behavioural patterns during the courtship over successive matings, the number of palpal insertions decreased. Unexpectedly, overall body condition did not decrease and males did not deplete their sperm supply. We found that 44% of the males were victims of sexual cannibalism after their third mating. The females that attacked or cannibalized males had less sperm stored in their spermathecae than those that did not. We discuss hypotheses that may clarify this scenario and the role of the cryptic female choice mechanism.

Effects of ovarian fluid on sperm traits and its implications for cryptic female choice in zebrafish

AbstractIn polyandrous mating systems, females maintain the opportunity to bias male fertilization success after mating in a process known as cryptic female choice. Mechanisms of cryptic female choice have been described both in internal and external fertilizers, and may affect fertilization processes at different stages before, during, and after fertilization. In internal fertilizers, females have substantial control over sperm storage and fertilization, whereas in external fertilizers, female control is limited. A key factor proposed to mediate cryptic female choice is the fluid surrounding the eggs, the ovarian fluid, as it may directly affect sperm performance. Here, we studied the role of ovarian fluid in post-mating sexual selection using the zebrafish, Danio rerio. Firstly, we assessed how ovarian fluid affects sperm swimming performance compared with freshwater. We focused on sperm motility, velocity, swimming trajectory, and longevity, all traits associated with competitive fertilization success in externally fertilizing fish. In a second step, we used a North Carolina II design to explore female, male, and female x male effects by testing sperm motility of 2 males in the ovarian fluid of 2 females in a total of 11 blocks. Our results indicate that the ovarian fluid affects sperm performance differently from freshwater. Specifically, sperm velocity, motility, and longevity were higher in the ovarian fluid than in freshwater, whereas sperm linearity and beat cross frequency showed the opposite pattern. Moreover, these effects varied according to male, female, and male x female identities, supporting the potential for cryptic female choice mediated by ovarian fluid in this species.

No evidence for prezygotic postcopulatory avoidance of kin despite high inbreeding depression.

Offspring resulting from mating among close relatives can suffer from impaired fitness through the expression of recessive alleles with deleterious effects. Postcopulatory sperm selection (a prezygotic mechanism of cryptic female choice) has been suggested to be an effective way to avoid inbreeding. To investigate whether postcopulatory female choice allows the avoidance of fertilization by close kin, we performed artificial inseminations in a promiscuous bird, the houbara bustard (Chlamydotis undulata undulata). Females were inseminated with a mix of sperm from triads of males, each constituted of a male genetically unrelated to the female, a first cousin and a half-sibling. When counting the number of eggs sired by unrelated males, cousins or half-siblings, we found a significant deviation from the expected random distribution, with more eggs sired by unrelated males. However, offspring sired by cousins, and especially by half-siblings suffered from high prehatching mortality, suggesting that the observed paternity skew towards unrelated males might reflect differential offspring mortality rather than sperm selection. In agreement with this hypothesis, within-triad siring success was similar for the three parental relatedness categories, but the relationship between siring and hatching success differed across categories. In clutches with high hatching success, unrelated males had the highest success while in clutches with high failure rate, half-siblings had the highest success. Offspring sired by half-siblings also suffered from reduced growth rate during the first three months and higher posthatching mortality. Hence, despite substantial fitness costs associated with fertilization by close relatives, females do not seem to select sperm of unrelated males.

Male-female relatedness at specific SNP-linkage groups influences cryptic female choice in Chinook salmon (Oncorhynchus tshawytscha).

In a range of taxa, the relatedness between mates influences both pre- and post-mating processes of sexual selection. However, relatively little is known about the genetic loci facilitating such a bias, with the exception of the major histocompatibility complex. Here, we performed tightly controlled replicated in vitro fertilization trials to explore the impact of relatedness on two possible mechanisms of cryptic female choice (CFC) in Chinook salmon (Oncorhynchus tshawytscha). We tested (i) whether relatedness of mates, assessed using 682 single nucleotide polymorphisms (SNPs) on 29 SNP-linkage groups (LGs), biases a male's sperm velocity in ovarian fluid (a parameter previously shown to predict male fertilization success), and (ii) whether relatedness of mates governs fertilization success via other mechanisms, probably via sperm-egg interactions. We found that relatedness on three LGs explained the variation in sperm velocity, and relatedness on two LGs explained fertilization success, which might indicate the presence of genes important in sperm-ovarian fluid and sperm-egg interactions in these genomic regions. Mapping of the SNPs on these LGs to the rainbow trout genome revealed two genes that affect fertility in humans and represent candidate genes for further studies. Our results thereby provide a novel contribution to the understanding of the mechanism of CFC.

Sexual selection for genetic compatibility: the role of the major histocompatibility complex on cryptic female choice in Chinook salmon (Oncorhynchus tshawytscha).

Cryptic female choice (CFC), a form of sexual selection during or post mating, describes processes of differential sperm utilization by females to bias fertilization outcomes towards certain males. In Chinook salmon (Oncorhynchus tshawytscha) the ovarian fluid surrounding the ova of a given female differently enhances the sperm velocity of males. Sperm velocity is a key ejaculate trait that determines fertilization success in externally fertilizing fishes, thus the differential effect on sperm velocity might bias male fertilization outcomes and represent a mechanism of CFC. Once sperm reach the oocyte, CFC could potentially be further facilitated by sperm-egg interactions, which are well understood in externally fertilizing marine invertebrates. Here, we explored the potential genetic basis of both possible mechanisms of CFC by examining whether the genotypic combinations of mates (amino-acid divergence, number of shared alleles) at the major histocompatibility complex (MHC) class I and II explain the variation in sperm velocity and/or male fertilization success that is not explained by sperm velocity, which might indicate MHC-based sperm-egg interactions. We recorded sperm velocity in ovarian fluid, employed paired-male fertilization trials and evaluated the fertilization success of each male using microsatellite-based paternity assignment. We showed that relative sperm velocity was positively correlated with fertilization success, confirming that the differential effect on sperm velocity may be a mechanism of CFC in Chinook salmon. The variation in sperm velocity was independent of MHC class I and II. However, the MHC class II divergence of mates explained fertilization success, indicating that this locus might influence sperm-egg interactions.

Multiple mechanisms of cryptic female choice act on intraspecific male variation in Drosophila simulans

Postcopulatory sexual selection can arise when females mate with multiple males and is usually mediated by an interaction between the sexes. Cryptic female choice (CFC) is one form of postcopulatory sexual selection that occurs when female morphology, physiology, or behavior generates a bias in fertilization success. However, its importance in nonrandom reproductive success is poorly resolved due to challenges distinguishing the roles of females and males in generating patterns of fertilization bias. Nevertheless, two CFC mechanisms have recently been documented and characterized in Drosophila simulans within the context of gametic isolation in competitive hybrid matings with Drosophila mauritiana: sperm ejection and nonrandom use of sperm storage organs for fertilization. Here, we explore if and how female D. simulans employ these two mechanisms of CFC in response to intraspecific male size variation. We used transgenic males expressing green (GFP) or red fluorescent protein (RFP) in sperm heads to document postcopulatory processes, in conjunction with a probabilistic analytical model. We unexpectedly found that differential reproductive success was also a function of male population (GFP or RFP), suggesting that females use different CFC mechanisms to select for different male traits. Moreover, concordance of selection at the precopulatory (as measured by mating latency) and postcopulatory stages depends on both the male trait and the CFC mechanism examined. Larger males were more successful both before and after mating, but we unexpectedly found that females also mated more quickly with males with GFP-labeled sperm, while fertilization bias favored RFP-labeled sperm.

Female effects, but no intrinsic male effects on paternity outcome in crickets.

Competitive fertilization success can depend on the relative abilities of competing males to fertilize available ova, and on mechanisms of cryptic female choice that moderate paternity. Competitive fertilization success is thus an emergent property of competing male genotypes, female genotype and their interactions. Accurate estimates of intrinsic male effects on competitive fertilization success are therefore problematic. We used a cross-classified nonbreeding design in which rival male family background was standardized to partition variation in competitive fertilization success among male and female family backgrounds in the field cricket Teleogryllus oceanicus. Male effects were close to zero, supporting previous quantitative genetic designs in which male competitors were assigned at random. In contrast, some 22% of the variance in competitive fertilization success was explained by female effects, suggesting that paternity in this species is influenced strongly by cryptic female choice.

Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behavior.

Despite evidence that variation in male–female reproductive compatibility exists in many fertilization systems, identifying mechanisms of cryptic female choice at the gamete level has been a challenge. Here, under risks of genetic incompatibility through hybridization, we show how salmon and trout eggs promote fertilization by conspecific sperm. Using in vitro fertilization experiments that replicate the gametic microenvironment, we find complete interfertility between both species. However, if either species’ ova were presented with equivalent numbers of both sperm types, conspecific sperm gained fertilization precedence. Surprisingly, the species’ identity of the eggs did not explain this cryptic female choice, which instead was primarily controlled by conspecific ovarian fluid, a semiviscous, protein-rich solution that bathes the eggs and is released at spawning. Video analyses revealed that ovarian fluid doubled sperm motile life span and straightened swimming trajectory, behaviors allowing chemoattraction up a concentration gradient. To confirm chemoattraction, cell migration tests through membranes containing pores that approximated to the egg micropyle showed that conspecific ovarian fluid attracted many more spermatozoa through the membrane, compared with heterospecific fluid or water. These combined findings together identify how cryptic female choice can evolve at the gamete level and promote reproductive isolation, mediated by a specific chemoattractive influence of ovarian fluid on sperm swimming behavior.

Promiscuity and elongated sperm storage organs work cooperatively as a cryptic female choice mechanism in an earwig

Female genitalia often show complex morphologies that cannot be explained by sperm reception and storage functions. However, our understanding of the forces underlying genital exaggeration in females is limited. Female earwigs, Euborellia plebeja , are promiscuous and their highly elongated sperm storage organs allow only partial removal and displacement of stored sperm by shorter male genitalia, resulting in only a 20% gain in paternity per copulation with a sperm-saturated female. This study examined the significance and optimality of restricted sperm displacement for females. A staged mating experiment with a paternity success analysis revealed that large males dominated male–male competition for burrows housing females, resulting in repeated copulations with the same female. Despite the low paternity gain per copulation, such repeated copulations resulted in a significant increase in paternity for larger males with higher resource-holding potential. A numerical simulation based on the relationship between male body size and copulation frequency showed that restricted sperm displacement (about 20% per copulation) is optimal for promiscuous females to accumulate sperm effectively from larger males. Because male body size is heritable in this species, females were estimated to benefit from a 1.4% increase in their sons' mating success. This genetic benefit disappeared when only a single copulation per male–female encounter was assumed. Since no measurable costs of mating for females have been detected in this species, the combination of promiscuity and restricted sperm displacement is best explained by the cryptic female choice hypothesis.

The effect of cryptic female choice on sex allocation in simultaneous hermaphrodites

Sex allocation theory for simultaneous hermaphrodites has focused primarily on the effects of sperm competition, but the role of mate choice has so far been neglected. We present a model to study the coevolution of cryptic female choice and sex allocation in simultaneous hermaphrodites. We show that the mechanism of cryptic female choice has a strong effect on the evolutionary outcome: if individuals remove a fixed proportion of less-preferred sperm, the optimal sex allocation is more female biased (i.e. more biased towards egg production) than without cryptic female choice; conversely, if a fixed amount of sperm is removed, sex allocation is less female-biased than without cryptic female choice, and can easily become male biased (i.e. biased towards sperm production). Under male-biased sex allocation, hermaphroditism can become unstable and the population can split into pure males and hermaphrodites with a female-biased allocation. We discuss the idea that the evolution of sex allocation may depend on the outcome of sexual conflict over the fate of received sperm: the sperm donor may attempt to manipulate or by-pass cryptic female choice and the sperm recipient is expected to resist such manipulation. We conclude that cryptic female choice can have a strong influence on sex allocation in simultaneous hermaphrodites and strongly encourage empirical work on this question.

Cryptic female choice by female control of oviposition timing in a soldier fly

There is substantial evidence that cryptic female choice (CFC) is present in numerous taxa. Several mechanisms have been proposed for CFC; however, we only have experimental evidence for a few of them. Female control of oviposition timing is a potentially widespread mechanism of CFC, but it has never been experimentally demonstrated. The aims of this study are to test 2 critical predictions of the hypothesis that CFC through control of oviposition timing occurs in the soldier fly Merosargus cingulatus: 1) to determine if M. cingulatus females are less likely to oviposit immediately after mating when the male does not perform copulatory courtship than when he does and 2) to determine if failure to immediately oviposit by the female results in lower reproductive success for the male she just mated with. To answer the first question, I compared the oviposition behavior of females that mated with control males versus females that mated with manipulated males that could not perform copulatory courtship. I showed that M. cingulatus females fail to oviposit immediately after copulation when males do not perform copulatory courtship. To answer the second question, I showed that there is last male sperm precedence in M. cingulatus. Because the last male to mate fertilizes most of the female’s eggs, a male will benefit when females oviposit immediately after mating with him and before remating with another male. Key words: copulatory courtship, cryptic female choice, oviposition timing, postcopulatory sexual selection, soldier fly, Stratiomyidae. [Behav Ecol]

Egg jelly influences sperm motility in the externally fertilizing frog,Crinia georgiana

Recent in vitro fertilization studies have revealed female and male x female interaction effects on the probability of fertilization. These findings suggest a mechanism of cryptic female choice via sperm-egg interactions. The egg jelly of anuran amphibians contains proteins that facilitate the chemoattraction and binding of sperm for fertilization. Here we show that egg jelly also influences the onset of motility and swimming velocity of motile sperm in the frog Crinia georgiana. Moreover, we found significant among female variation in the effects of egg jelly on sperm motility. We discuss this finding with respect to male and female effects on nonrandom fertilization observed in this species.

Differential survival of allosperm by location within the female storage organ of the snail Cornu aspersum

The sperm storage organ of terrestrial gastropod molluscs is implicated in sexual selection because it has a complex structure and it functions in a context of intense sperm competition. Received sperm are stored in spermathecal tubules. In our sample using the brown garden snail ( Cornu aspersum (Müller, 1774)) (n = 58), the mean number of tubules per animal was 16, with lengths ranging from ≤40 to 2480 μm. A hereditary influence on tubule number was indicated by clutch-dependent variations. From histological sections, we counted the spermatozoa that were present in the tubules of ex-virgin snails 1, 2, 4, and 8 weeks after mating (n = 40). Sperm were distributed, on average, across 75% of the tubules in individual snails, thus contradicting one proposed mechanism for cryptic female choice. The total number of sperm declined 66% over 8 weeks, with the largest losses incurred by sperm in the lumens of the tubules and sperm gathered in clusters. By contrast, in the same period, the numbers of sperm that were in contact with the walls of the tubules remained relatively stable. These data imply that sperm survive best when attached to the epithelial wall, either because they derive nutrition from the epithelium or because they use the epithelium as an anchor.

A mechanism for cryptic female choice in chinook salmon

Female mate choice after copulation or spawning is cryptic when a female differentially influences the fertilization success of sperm from different males. We tested whether ovarian fluid could act as a potential mechanism of cryptic female choice (CFC) in chinook salmon (Oncorhynchus tshawytscha) by comparing how ovarian fluid from each of 7 females affected the sperm behavior of 11 different males. Using computer-assisted sperm analysis, we measured sperm velocity, motility, longevity, and linearity from the ejaculates of each male activated in the ovarian fluid from each female. Mean sperm swimming speed, path trajectory, and longevity differed significantly among males, and within males depended on the female’s ovarian fluid in which it was activated. Most important, the pattern of within-male variation in these traits also varied significantly among males in response to different females’ ovarian fluids. As sperm velocity is known to be a prime determinant of fertilization success in externally fertilizing fishes. This finding suggests that variation in the composition of female ovarian fluid may be a mechanism for CFC, whereby females differentially enhance the swimming speed of sperm from different males. Thus, female ovarian fluid can alter relative male fertilization success when there is intense sperm competition, as there is in this and other group spawning fish species. Key words: chinook salmon, cryptic female choice, Oncorhynchus tshawytshca, ovarian fluid, sperm traits, sperm velocity. [Behav Ecol]

Copulation duration, insemination efficiency and male attractiveness in guppies

In polyandrous species, females may influence paternity by biasing sperm usage in favour of particular males. In the guppy, Poecilia reticulata, the number of sperm inseminated in a copulation depends on the female's perception of male attractiveness. We videorecorded copulations in the laboratory to test the hypothesis that there is a positive correlation between the number of sperm inseminated and the duration of the copulation. Duration was positively correlated with the number of sperm retrieved from the female's gonoduct. Once copulation duration was statistically controlled for, more sperm were retrieved from the gonoduct in courtship copulations than in coercive copulations, and in postpartum females than in virgin females. Copulation duration was positively correlated with the degree of carotenoid coloration of the male, suggesting that copulation duration might be the proximate mechanism of cryptic female choice in this species. The intensity of ‘jerking’, a postcopulatory behaviour of male guppies, was positively correlated with the number of sperm inseminated, suggesting a possible signalling function of this display.

Cryptic female choice during spermatophore transfer in Tribolium castaneum (Coleoptera: Tenebrionidae)

Sexual selection in both males and females promotes traits and behaviors that allow control over paternity when female mates with multiple males. Nonetheless, mechanisms of cryptic female choice have been consistently overlooked, due to traditional focus on sperm competition as well as difficulty in distinguishing male vs. female influence over processes occurring during and after mating. The first part of this study describes morphology and transformation of Tribolium castaneum spermatophores inferred from dissecting females immediately after normal or interrupted copulations. T. castaneum males are found to transfer spermatophores as an invaginated tube that everts inside the female bursa and which is filled with sperm during copulation. This sequence of events makes it feasible for females to control the sperm quantity transferred in each spermatophore. Through manipulation of the male phenotypic quality (by starvation) and manipulation of female control over sperm transfer (by killing a subset of females), the second part of this study examines whether females use control over transferred sperm quantity as a cryptic choice mechanism. Fed males transferred significantly more sperm per spermatophore than starved males but only when mating with live females. These results suggest an active differentiation by live females against starved males and provide an evidence for the proposed cryptic female choice mechanism.

Sperm ejection as a possible cryptic female choice mechanism in Odonata (Insecta)

Abstract. The few odonate studies of sperm use suggest that females spend apparently more sperm than appears necessary during oviposition (sometimes females may have their sperm stores reduced to 50% after a single oviposition episode). Furthermore, some studies document that females eject sperm during and after copulation. This raises the question of whether sperm reduction may be interpreted as a cryptic female choice mechanism. Using two zygopterans, Ischnura denticollis Burmeister and Enallagma praevarum Hagen, and one anisopteran, Pantala flavescens Fabricius, it is shown that females mate more than once, show a marked reduction in stored sperm, and that this is by ejection of sperm before to oviposition. The extent of sperm reduction is inversely related to the number of eggs laid. When mated to the same male, females show similar reductions in sperm stores and egg load and only rarely does the vaginal duct contain sperm. This suggests that marked sperm reduction is common in this insect order and is not explained by an excess of sperm obstructing the egg passage. It is suggested that female's sperm shortage is better explained as a cryptic female choice mechanism aimed at favouring the sperm of some males. This study provides exciting research avenues for future studies of female choice in an animal taxa whose sexual biology is otherwise regarded as controlled by males.

How Important Is Sexual Conflict?

Next article No AccessHow Important Is Sexual Conflict?David Hosken and Rhonda SnookDavid Hosken Search for more articles by this author and Rhonda Snook Search for more articles by this author 1. Centre for Ecology and Conservation, University of Exeter in Cornwall, Tremough, Penryn, Cornwall TR10 9EZ, United Kingdom;2. Department of Animal and Plant Sciences, Alfred Denny Building, University of Sheffield, Western Bank, Sheffield S10 2TN, United KingdomPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 165, Number S5May 2005HOW IMPORTANT IS SEXUAL CONFLICT?A Special Issue Edited by David Hosken and Rhonda Snook Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/429355 Views: 112Total views on this site Citations: 25Citations are reported from Crossref © 2005 by The University of Chicago.PDF download Crossref reports the following articles citing this article:Marcus Lee, Carlota Solano Udina, Lars-Anders Hansson Fear of sex: sexual conflict exposed as avoidance in a parthenogenetic invertebrate, Behavioral Ecology and Sociobiology 75, no.88 (Jul 2021).https://doi.org/10.1007/s00265-021-03054-9David J. Hosken, C. 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How Important Is Sexual Conflict?

Next article No AccessHow Important Is Sexual Conflict?David Hosken and Rhonda SnookDavid Hosken Search for more articles by this author and Rhonda Snook Search for more articles by this author 1. Centre for Ecology and Conservation, University of Exeter in Cornwall, Tremough, Penryn, Cornwall TR10 9EZ, United Kingdom;2. Department of Animal and Plant Sciences, Alfred Denny Building, University of Sheffield, Western Bank, Sheffield S10 2TN, United KingdomPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 165, Number S5May 2005HOW IMPORTANT IS SEXUAL CONFLICT?A Special Issue Edited by David Hosken and Rhonda Snook Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/429355 Views: 127Total views on this site Citations: 25Citations are reported from Crossref © 2005 by The University of Chicago.PDF download Crossref reports the following articles citing this article:Marcus Lee, Carlota Solano Udina, Lars-Anders Hansson Fear of sex: sexual conflict exposed as avoidance in a parthenogenetic invertebrate, Behavioral Ecology and Sociobiology 75, no.88 (Jul 2021).https://doi.org/10.1007/s00265-021-03054-9David J. Hosken, C. Ruth Archer, Clarissa M. House, Nina Wedell Penis evolution across species: divergence and diversity, Nature Reviews Urology 16, no.22 (Nov 2018): 98–106.https://doi.org/10.1038/s41585-018-0112-zRebecah E. Ford, Stephen C. Weeks, E. Hebets Intersexual conflict in androdioecious clam shrimp: Do androdioecious hermaphrodites evolve to avoid mating with males?, Ethology 124, no.55 (Apr 2018): 357–364.https://doi.org/10.1111/eth.12738Linda C. Hernández Duran, Gonzalo E. Fajardo Medina, Luz S. Fuentes Quintero Mating Opportunities in Sangalopsis veliterna Females: Costs and Benefits, Journal of Insect Science 14, no.112112 (Aug 2014): 1–9.https://doi.org/10.1673/031.014.112Akanksha Singh, Bashisth N. Singh Role of sexual selection in speciation in Drosophila, Genetica 142, no.11 (Dec 2013): 23–41.https://doi.org/10.1007/s10709-013-9751-4Krista M. Milich, Janice M. Bahr, Rebecca M. Stumpf, Colin A. 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