scholarly journals Conspecific sperm precedence in Callosobruchus subinnotatus (Coleoptera: Bruchidae): mechanisms and consequences

2007 ◽  
Vol 274 (1612) ◽  
pp. 983-988 ◽  
Author(s):  
Paul F Rugman-Jones ◽  
Paul E Eady

Conspecific sperm precedence (CSP) has been identified as an important post-copulatory, pre-zygotic mechanism that can act to reduce gene flow between populations. The evolution of CSP is thought to have arisen as a by-product of male and female coevolution in response to intraspecific post-copulatory sexual selection. However, little is known about the mechanisms that generate CSP. When Callosobruchus subinnotatus females copulate with both C. subinnotatus and Callosobruchus maculatus males, regardless of mating order, the majority of eggs are fertilized by conspecific sperm. The low number of heterospecific fertilizations does not result from general differences in the viability of sperm in the female reproductive tract, as heterospecific sperm fertilized equivalent numbers of eggs as conspecific sperm in the absence of sperm competition. Instead, CSP results from disadvantages to heterospecific sperm that are manifest only when in competition with conspecific sperm. CSP in C. subinnotatus appears to result from two, not mutually exclusive, mechanisms. First, conspecific sperm are better able to displace heterospecific sperm from female storage. Second, conspecific sperm achieve disproportionately higher numbers of fertilizations relative to their proportional representation in the fertilization set. Thus, we provide evidence of differential sperm use from the female spermatheca.

2020 ◽  
Vol 375 (1813) ◽  
pp. 20200071 ◽  
Author(s):  
Martin D. Garlovsky ◽  
Leeban H. Yusuf ◽  
Michael G. Ritchie ◽  
Rhonda R. Snook

Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here , we show conpopulation sperm precedence (CpSP) between Drosophila montana populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation. This article is part of the theme issue ‘Fifty years of sperm competition’.


2020 ◽  
Author(s):  
Martin D. Garlovsky ◽  
Leeban H. Yusuf ◽  
Michael G. Ritchie ◽  
Rhonda R. Snook

ABSTRACTPostcopulatory sexual selection can generate coevolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilisation success diverge between populations postmating prezygotic barriers to gene flow may evolve. Conspecific sperm precedence is a form of such isolation thought to evolve early during speciation yet has mostly been studied between species. Here we show conpopulation sperm precedence between Drosophila montana populations. Using genomic data to estimate divergence times and patterns of gene flow between populations, we show gene flow has played a considerable role during divergence. We find conpopulation sperm precedence is asymmetric and is concordant with asymmetry in non-competitive postmating prezygotic reproductive isolation. These results suggest these phenomena have a shared mechanism, but we show that this asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilisation success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of postmating prezygotic reproductive isolation. We suggest that divergence of postcopulatory phenotypes resulting in postmating prezygotic isolation is potentially driven by cryptic female choice, or mutation order divergence.


Author(s):  
Patricia L.R. Brennan ◽  
Dara N. Orbach

The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.


Behaviour ◽  
2006 ◽  
Vol 143 (5) ◽  
pp. 643-658 ◽  
Author(s):  
Ludovic Arnaud ◽  
Giorgina Bernasconi ◽  
Yves Brostaux ◽  
Eric P. Meyer

AbstractIn polyandrous insects, postcopulatory sexual selection is a pervasive evolutionary force favouring male and female traits that allow control of offspring paternity. Males may influence paternity through adaptations for sperm competition, and females through adaptations facilitating cryptic female choice. Yet, the mechanisms are often complex, involving behaviour, physiology or morphology, and they are difficult to identify. In red flour beetles (Tribolium castaneum), paternity varies widely, and evidence suggests that both male and female traits influence the outcome of sperm competition. To test the role of spermathecal morphology and of sperm storage processes on the outcome of sperm competition, we mated each of 26 virgin females with two males, one of which carrying a phenotypic marker to assign offspring paternity. We manipulated the interval between mating with the first and the second male, to create different conditions of sperm storage (overlapping and non-overlapping) in the female reproductive tract. To investigate the role of sperm storage more closely, we examined the relationship between paternity and spermathecal morphology in a subset of 14 experimental females. In addition, we also characterized variation in spermathecal morphology in three different strains, wildtype, Chicago black and Reindeer. No significant influence of the intermating interval was found on the paternity of the focal male, although the direction of the difference was in the expected direction of higher last male paternity for longer intervals. Moreover, paternity was not significantly associated with spermathecal morphology, although spermathecal volume, complexity, and tubule width varied significantly and substantially among individuals in all investigated strains.


2020 ◽  
Author(s):  
Kristin A. Hook ◽  
W. David Weber ◽  
Heidi S. Fisher

AbstractIn some species, sperm form motile, coordinated groups as they migrate through the female reproductive tract. Collective sperm migration is posited to have evolved to improve sperm swimming performance, and thus may be beneficial in a competitive context, but limited evidence supports this theory. Here we investigate sperm aggregation across closely-related species of Peromyscus mice that naturally vary by mating system. We find that phylogenetic history predicts the likelihood that sperm will aggregate but that variation in aggregate size negatively associates with relative testis size, suggesting that sperm competition has a stabilizing effect on this trait. Moreover, we show that sperm aggregation is not kinematically beneficial for all species, and we hypothesize that swimming performance is dependent on the orientation and composition of sperm groups. To test this, we compared sperm from the two sister-species that aggregate most frequently and find that sperm of the species that evolved under intense sperm competition forms aggregates with efficient geometry more frequently than sperm from its monogamous congener. Together, our results are consistent with the hypothesis that sperm aggregation evolved to improve motility in a competitive context; however, when monogamy evolved secondarily, relaxed sexual selection allowed for less efficient strategies to persist.


2021 ◽  
Author(s):  
Paris Veltsos ◽  
Damiano Porcelli ◽  
Yongxiang Fang ◽  
Andrew R. Cossins ◽  
Michael G. Ritchie ◽  
...  

AbstractMating causes substantial changes in females, altering male and female reproductive fitness. Some postmating effects are hypothesized to be at least partially mediated by gene expression changes, driven by postcopulatory sexual selection, which results in population divergence of reproductive proteins that could generate reproductive isolation. However, understanding of the direct role of sexual selection on gene expression divergence along with the subsequent molecular mismatches that could occur between diverging populations is limited. Here, we analyze gene expression divergence following over 150 generations of experimental evolution in which Drosophila pseudoobscura evolved under either elevated polyandry or enforced monogamy. We find that sexual selection rapidly impacted sex-, tissue-, and mating-specific responses, and not always in the predicted direction. Postmating female responses are either unique to each sexual selection treatment or exhibit asymmetric non-congruence, in which monogamy females upregulate and polyandry females downregulate the same genes following mating. This substantial population divergence of gene expression also gives rise to either unique or mismatched gene expression patterns in crosses between treatments. Many of these genes are involved in immune and stress responses, and non-congruent responses are particularly prevalent in the female reproductive tract, the main arena for postcopulatory sexual selection. In summary, we show that sexual selection has pervasive impacts on gene expression divergence acting both differentially between reproductive tissues of the same sex and asymmetrically in postmating female responses, and this divergence is highest in the female reproductive tract, the main arena for postcopulatory sexual selection.


Author(s):  
Zachariah Wylde ◽  
Angela Crean ◽  
Russell Bonduriansky

Abstract Ejaculate traits can be sexually selected and often exhibit heightened condition-dependence. However, the influence of sperm competition risk in tandem with condition-dependent ejaculate allocation strategies is relatively unstudied. Because ejaculates are costly to produce, high-condition males may be expected to invest more in ejaculates when sperm competition risk is greater. We examined the condition-dependence of ejaculate size by manipulating nutrient concentration in the juvenile (larval) diet of the neriid fly Telostylinus angusticollis. Using a fully factorial design we also examined the effects of perceived sperm competition risk (manipulated by allowing males to mate first or second) on the quantity of ejaculate transferred and stored in the three spermathecae of the female reproductive tract. To differentiate male ejaculates, we fed males nontoxic rhodamine fluorophores (which bind to proteins in the body) prior to mating, labeling their sperm red or green. We found that high-condition males initiated mating more quickly and, when mating second, transferred more ejaculate to both of the female’s posterior spermathecae. This suggests that males allocate ejaculates strategically, with high-condition males elevating their ejaculate investment only when facing sperm competition. More broadly, our findings suggest that ejaculate allocation strategies can incorporate variation in both condition and perceived risk of sperm competition.


2020 ◽  
Vol 375 (1813) ◽  
pp. 20200062
Author(s):  
Leigh W. Simmons ◽  
Geoff A. Parker ◽  
David J. Hosken

Studies of the yellow dungfly in the 1960s provided one of the first quantitative demonstrations of the costs and benefits associated with male and female reproductive behaviour. These studies advanced appreciation of sexual selection as a significant evolutionary mechanism and contributed to the 1970s paradigm shift toward individual selectionist thinking. Three behaviours in particular led to the realization that sexual selection can continue during and after mating: (i) female receptivity to remating, (ii) sperm displacement and (iii) post-copulatory mate guarding. These behaviours either generate, or are adaptations to sperm competition, cryptic female choice and sexual conflict. Here we review this body of work, and its contribution to the development of post-copulatory sexual selection theory. This article is part of the theme issue ‘Fifty years of sperm competition’.


2006 ◽  
Vol 274 (1607) ◽  
pp. 247-252 ◽  
Author(s):  
Paul E Eady ◽  
Leticia Hamilton ◽  
Ruth E Lyons

Antagonistic sexual coevolution stems from the notion that male and female interests over reproduction are in conflict. Such conflicts appear to be particularly obvious when male genital armature inflicts damage to the female reproductive tract resulting in reduced female longevity. However, studies of mating frequency, genital damage and female longevity are difficult to interpret because females not only sustain more genital damage, but also receive more seminal fluid when they engage in multiple copulations. Here, we attempt to disentangle the effects of genital damage and seminal fluid transfer on female longevity in the beetle Callosobruchus maculatus (Coleoptera: Bruchidae). Males copulating for the sixth time in succession inflicted greater levels of genital damage, but transferred smaller ejaculates in comparison with virgin males. The number of copulations performed by males was negatively related to female fecundity and positively related to female longevity, suggesting a trade-off between fecundity and longevity. However, inclusion of fecundity as a covariate revealed sperm and/or seminal fluid transfer to have a negative impact on female longevity above that caused by the fecundity–longevity trade-off. The consequences of multiple copulations on female longevity were examined. Females that mated twice laid more eggs and died sooner than those that mated once. However, incorporation of fecundity as a covariate into our statistical model removed the effect of female mating frequency on female longevity, indicating that double-mated females suffer greater mortality owing to the trade-off between fecundity and longevity. Males of this species are known to transfer very large ejaculates (up to 8% of their body weight), which may represent a significant nutritional benefit to females. However, the receipt of large ejaculates appears to carry costs. Thus, the interpretation of multiple mating experiments on female longevity and associated functional explanations of polyandry in this species are likely to be complex.


2017 ◽  
Vol 284 (1855) ◽  
pp. 20170132 ◽  
Author(s):  
Liam R. Dougherty ◽  
Emile van Lieshout ◽  
Kathryn B. McNamara ◽  
Joe A. Moschilla ◽  
Göran Arnqvist ◽  
...  

Traumatic mating (or copulatory wounding) is an extreme form of sexual conflict whereby male genitalia physically harm females during mating. In such species females are expected to evolve counter-adaptations to reduce male-induced harm. Importantly, female counter-adaptations may include both genital and non-genital traits. In this study, we examine evolutionary associations between harmful male genital morphology and female reproductive tract morphology and immune function across 13 populations of the seed beetle Callosobruchus maculatus . We detected positive correlated evolution between the injuriousness of male genitalia and putative female resistance adaptations across populations. Moreover, we found evidence for a negative relationship between female immunity and population productivity, which suggests that investment in female resistance may be costly due to the resource trade-offs that are predicted between immunity and reproduction. Finally, the degree of female tract scarring (harm to females) was greater in those populations with both longer aedeagal spines and a thinner female tract lining. Our results are thus consistent with a sexual arms race, which is only apparent when both male and female traits are taken into account. Importantly, our study provides rare evidence for sexually antagonistic coevolution of male and female traits at the within-species level.


Sign in / Sign up

Export Citation Format

Share Document