Asymmetries in reproductive anatomy: insights from promiscuous songbirds

Abstract Directional asymmetry in gonad size is commonly observed in vertebrates and is particularly pronounced in birds, where the left testis is frequently larger than the right. The adaptive significance of directional asymmetry in testis size is poorly understood, and whether it extends beyond the testes (i.e. side-correspondent asymmetry along the reproductive tract) has rarely been considered. Using the Maluridae, a songbird family exhibiting variation in levels of sperm competition and directional testis asymmetry, yet similar in ecology and life history, we investigated the relative roles of side-correspondence and sperm competition on male reproductive tract asymmetry at both inter- and intraspecific levels. We found some evidence for side-correspondent asymmetry. Additionally, sperm competition influenced directional asymmetry at each end of the reproductive tract: species experiencing higher levels of sperm competition had a relatively larger right testis and relatively more sperm in the right seminal glomerus. Within red-backed fairy-wrens (Malurus melanocephalus), auxiliary males had relatively more sperm in the left seminal glomerus, in contrast to a right-bias asymmetry throughout the reproductive tract in breeding males. Given that the number of sperm is important for competitive fertilization success, our results suggest that sperm competition shapes reproductive asymmetries beyond testis size, with likely functional consequences for male reproductive success.

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Effects on differentiation of reproductive organs and sexual behaviour in Japanese quail by excessive embryonic ERα activation

Reproduction Fertility and Development ◽

10.1071/rd08293 ◽

2010 ◽

Vol 22 (2) ◽

pp. 416 ◽

Cited By ~ 6

Author(s):

Anna Mattsson ◽

Björn Brunström

Keyword(s):

Japanese Quail ◽

Oestrogen Receptor ◽

Reproductive Tract ◽

Reproductive Organs ◽

Positive Control ◽

Reproductive Organ ◽

Testis Size ◽

Left Testis ◽

The Right ◽

Copulatory Behaviour

Exposure of Japanese quail (Coturnix japonica) embryos to oestrogenic substances disrupts sexual differentiation of the reproductive tract of both sexes and impairs the copulatory behaviour of the adult male. To examine whether these effects can be induced by selective activation of oestrogen receptor α (ERα), Japanese quail eggs were injected with various doses of the selective ERα agonist 16α-lactone-oestradiol (16α-LE2). The natural oestrogen 17β-oestradiol (E2) was used as a positive control. Both 16α-LE2 and E2 induced formation of an ovary-like cortex in the left testis (ovotestis) and reduced the size of the right testis in male embryos. The asymmetry in testis size remained in sexually mature males. Both substances induced retention and malformation of the Müllerian ducts in embryos of both sexes and malformed oviducts in juveniles. Male copulatory behaviour was suppressed by embryonic exposure to E2 and the highest dose of 16α-LE2. However, the lower dose of 16α-LE2, which markedly affected development of the reproductive organs, was without effects on behaviour. It can therefore not be excluded that the behavioural demasculinisation at the 100-fold higher dose involved cross-activation of oestrogen receptor β (ERβ). In conclusion, our results suggest that oestrogen-induced disruption of reproductive organ development in Japanese quail can be mediated via ERα, whereas the role of ERα in demasculinisation of copulatory behaviour remains to be clarified.

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Post-Copulatory Sexual Selection

Evolutionary Biology ◽

10.1093/obo/9780199941728-0131 ◽

2021 ◽

Author(s):

Patricia L.R. Brennan ◽

Dara N. Orbach

Keyword(s):

Sexual Selection ◽

Sperm Competition ◽

Female Choice ◽

Reproductive Tract ◽

Seminal Fluid ◽

Fertilization Success ◽

Female Reproductive Tract ◽

Cryptic Female Choice ◽

Trade Offs ◽

Morphological Criteria

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.

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Testicular Volume and Asymmetry are Age-Dependent in Black-Throated Blue Warblers (Dendroica Caerulescens)

The Auk ◽

10.1093/auk/121.2.473 ◽

2004 ◽

Vol 121 (2) ◽

pp. 473-485

Author(s):

Gary R. Graves

Keyword(s):

Sperm Competition ◽

Testicular Volume ◽

Directional Asymmetry ◽

Left Testis ◽

Extrapair Paternity ◽

Dendroica Caerulescens ◽

Julian Date ◽

Age Dependent ◽

Testicular Morphology ◽

Older Males

Abstract Passerine birds are favored models for studies of sperm competition and extrapair paternity, yet the intraspecific chronology of testicular maturation and its empirical and theoretical consequences in avian mating systems have been largely ignored. I analyzed age-dependent variation in testicular morphology in 25 breeding populations of the Black-throated Blue Warbler (Dendroica caerulescens) distributed throughout its geographic range in eastern North America. Yearlings (first breeding season) had significantly smaller testes than older males (≥2 years). Latitude, altitude, and Julian date had negligible effects on testicular morphology when effects of core body size were controlled. Preparator effects had significant influence on the estimation of testicular volume and asymmetry. Contrary to Moller's hypothesis that the smaller testis compensates for deficiencies in the larger, the volumes of the left and right testes were positively correlated in both yearlings and older males. Older males exhibited a higher degree of directional asymmetry because of the disproportionate enlargement of the left testis. These data suggest that testicular morphology and reproductive capacities of yearling passerines may not be equivalent to those of older males. In a broader context, these findings demonstrate that age class should be factored into quantitative models of sperm competition in birds.

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Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster.

Genetics ◽

10.1093/genetics/139.1.189 ◽

1995 ◽

Vol 139 (1) ◽

pp. 189-201 ◽

Cited By ~ 15

Author(s):

A G Clark ◽

M Aguadé ◽

T Prout ◽

L G Harshman ◽

C H Langley

Keyword(s):

Reproductive Tract ◽

Seminal Fluid ◽

Glucose Dehydrogenase ◽

Natural Populations ◽

Fertilization Success ◽

Accessory Gland ◽

Male Reproductive Success ◽

Sperm Displacement ◽

Naturally Occurring ◽

Accessory Gland Protein

Abstract Genes that influence mating and/or fertilization success may be targets for strong natural selection. If females remate frequently relative to the duration of sperm storage and rate of sperm use, sperm displacement may be an important component of male reproductive success. Although it has long been known that mutant laboratory stocks of Drosophila differ in sperm displacement, the magnitude of the naturally occurring genetic variation in this character has not been systematically quantified. Here we report the results of a screen for variation in sperm displacement among 152 lines of Drosophilia melanogaster that were made homozygous for second and/or third chromosomes recovered from natural populations. Sperm displacement was assayed by scoring the progeny of cn;bw females that had been mated sequentially to cn;bw and tested males in either order. Highly significant differences were seen in both the ability to displace sperm that is resident in the female's reproductive tract and in the ability to resist displacement by subsequent sperm. Most lines exhibited nearly complete displacement, having nearly all progeny sired by the second male, but several lines had as few as half the progeny fathered by the second male. Lines that were identified in the screen for naturally occurring variation in sperm displacement were also characterized for single-strand conformation polymorphisms (SSCP) at seven accessory gland protein (Acp) genes, Glucose dehydrogenase (Gld), and Esterase-6 (Est-6). Acp genes encode proteins that are in some cases known to be transmitted to the female in the seminal fluid and are likely candidates for genes that might mediate the phenomenon of sperm displacement. Significant associations were found between particular Acp alleles at four different loci (Acp26Aa/Ab, Acp29B, Acp36DE and Acp53E) and the ability of males to resist displacement by subsequent sperm. There was no correlation between the ability to displace resident sperm and the ability to resist being displaced by subsequent sperm. This lack of correlation, and the association of Acp alleles with resisting subsequent sperm only, suggests that different mechanisms mediate the two components of sperm displacement.

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Sperm competition in squamate reptiles

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0079 ◽

2020 ◽

Vol 375 (1813) ◽

pp. 20200079

Author(s):

Christopher R. Friesen ◽

Ariel F. Kahrl ◽

Mats Olsson

Keyword(s):

Sperm Competition ◽

Reproductive Tract ◽

Multiple Paternity ◽

Fertilization Success ◽

Sperm Storage ◽

Female Reproductive Tract ◽

Life History Strategies ◽

The Face ◽

And Function ◽

Sperm Size

Multiple paternity is ubiquitous within the polyphyletic group called ‘reptiles', especially within the lizards and snakes. Therefore, the probability of sperm competition occurring, and being intense, is high. Squamates exhibit a diversity of tactics to ensure fertilization success in the face of sperm competition. The duration of female sperm storage, which can be many months and even years in some species, remains an enigma. Here, we emphasize some mechanisms that might affect patterns of paternity, the source and function of ejaculates and features of the female reproductive tract that may aid in long-term sperm storage. In doing so, we present a new analysis of the relationship between sperm size, the strength of sperm competition and the duration of female sperm storage. Lizards and snakes are a diverse group that has provided many excellent models for the study of an array of life-history strategies. However, when it comes to postcopulatory sexual selection, there is much left to discover. This article is part of the theme issue ‘Fifty years of sperm competition'.

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Collective sperm movements in Peromyscus mice are shaped by phylogenetic history and post-copulatory sexual selection

10.1101/2020.02.08.939975 ◽

2020 ◽

Author(s):

Kristin A. Hook ◽

W. David Weber ◽

Heidi S. Fisher

Keyword(s):

Sexual Selection ◽

Sperm Competition ◽

Reproductive Tract ◽

Swimming Performance ◽

Aggregate Size ◽

Female Reproductive Tract ◽

Testis Size ◽

Limited Evidence ◽

Closely Related Species ◽

Sperm Migration

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.

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Sperm Numbers as a Paternity Guard in a Wild Bird

Cells ◽

10.3390/cells11020231 ◽

2022 ◽

Vol 11 (2) ◽

pp. 231

Author(s):

Melissah Rowe ◽

Annabel van Oort ◽

Lyanne Brouwer ◽

Jan T. Lifjeld ◽

Michael S. Webster ◽

...

Keyword(s):

Reproductive Success ◽

Sperm Competition ◽

Ecological Factors ◽

Fertilization Success ◽

Male Reproductive Success ◽

Male Mating ◽

Sexually Selected Traits ◽

Paternity Success ◽

Mating Conditions ◽

Sperm Traits

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male’s ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success.

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Genetic coordination of sperm morphology and seminal fluid proteins promotes male reproductive success in Drosophila melanogaster

10.1101/2021.11.15.468624 ◽

2021 ◽

Author(s):

Jake Galvin ◽

Erica Larson ◽

Sevan Yedigarian ◽

Mohammad Rahman ◽

Kirill Borziak ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Reproductive Success ◽

Sperm Competition ◽

Seminal Fluid ◽

Fertilization Success ◽

Male Reproductive Success ◽

Sperm Length ◽

Seminal Fluid Proteins ◽

Female Remating ◽

Paternity Success

Spermatozoal morphology is highly variable both among and within species and in ways that can significantly impact fertilization success. In Drosophila melanogaster, paternity success depends on sperm length of both competing males and length of the female's primary sperm storage organ. We found that genes upregulated in long sperm testes are enriched for lncRNAs and seminal fluid proteins (Sfps). Transferred in seminal fluid to the female during mating, Sfps are secreted by the male accessory glands (AG) and affect female remating rate, physiology, and behavior with concomitant advantages for male reproductive success. Despite being upregulated in long sperm testes, they have no known function in testis tissue. We found that Sex Peptide and ovulin (Acp26Aa) knockouts resulted in shorter sperm, suggesting that Sfps may regulate sperm length during spermatogenesis. However, knockout of AG function did not affect sperm length, suggesting that AG expression has no influence on spermatogenic processes. We also found that long sperm males are better able to delay female remating, suggesting higher Sfp expression in AG. These results might suggest that long sperm males have a double advantage in sperm competition by both delaying female remating, likely through transfer of more Sfps, and by resisting sperm displacement. However, we also found that this extra advantage does not necessarily translate to more progeny or higher paternity success. Thus, we found that multiple components of the ejaculate coordinate to promote male reproductive success at different stages of reproduction, but the realized fitness advantages in sperm competition are uncertain.

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PSX-5 Reproductive organ weights, morphology and sperm reserves in intact and short scrotum post-pubertal male dairy sheep lambs

Journal of Animal Science ◽

10.1093/jas/skz258.920 ◽

2019 ◽

Vol 97 (Supplement_3) ◽

pp. 467-467

Author(s):

Stephan Wildeus ◽

Susan Schoenian ◽

D Philip Sponenberg ◽

Mary Beth Bennett ◽

Dahlia O’Brien

Keyword(s):

Reproductive Tract ◽

Reproductive Organ ◽

Sperm Production ◽

Dairy Sheep ◽

Left Testis ◽

Significant Difference ◽

Ram Lambs ◽

The Right ◽

Tubule Diameter ◽

Daily Sperm Production

Abstract This study evaluated the use of short-scrotum castration to create sterile ram lambs. East Friesian x Lacaune male lambs born in February on a commercial sheep dairy were left intact (n = 19; IN) or rendered short-scrotum (n = 17; SS) within 10 d of birth. At 3 mo of age lambs were transferred to the study site and grazed as one group, while being supplemented with a grain mixture at 0.7 kg/d. Lambs were harvested at 6 mo of age, and reproductive tract of 5 IN and 5 SS lambs collected at random and shipped cold overnight for processing. Testis and epididymis were weighed. Segments of the left testis and epididymis were processed for histology, while a subsample of testicular parenchyma and epididymal segments of the right side were used to determine sperm reserves by tissue homogenization. Differences between testis types were determined using GLM of SAS. Testes and epididymal weights were reduced (P < 0.001) in SS (115 and 22 g) compared to IN (364 and 50 g) lambs. Seminiferous tubule diameter was also smaller (P < 0.001) in SS (142 µm) than IN (234 µm) lambs. Daily sperm production per gram testicular parenchyma (DSPG) was not different between types (3.8 vs. 2.3 million sperm/g; P = 0.06), but total daily sperm production was lower (P < 0.01) in SS (0.23 billion) than IN (1.34 billion) ram lambs. Considerable variation was noted in DSPG in IN lambs suggesting still incomplete development at this age, and accounting for the lack of a significant difference. Epididymal sperm reserves were markedly reduced (P < 0.001) in SS (0.1 billion) compared to IN (10.5 billion), and decreased along the epididymis, supported by evidence of phagocytic action by the epididymal epithelium. Data suggest that ram lambs rendered short-scrotum shortly after birth develop smaller testes with reduced sperm production, making them effectively infertile.

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Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0071 ◽

2020 ◽

Vol 375 (1813) ◽

pp. 20200071 ◽

Cited By ~ 1

Author(s):

Martin D. Garlovsky ◽

Leeban H. Yusuf ◽

Michael G. Ritchie ◽

Rhonda R. Snook

Keyword(s):

Sexual Selection ◽

Gene Flow ◽

Sperm Competition ◽

Reproductive Tract ◽

Fertilization Success ◽

Female Reproductive Tract ◽

Sperm Precedence ◽

Arms Races ◽

Postcopulatory Sexual Selection ◽

The Face

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’.

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