The Reproductive Microbiome: An Emerging Driver of Sexual Selection, Sexual Conflict, Mating Systems, and Reproductive Isolation

Trends in Ecology & Evolution, Journal Year: 2020, Volume and Issue: 35(3), P. 220 - 234

Published: Jan. 14, 2020

Although it is clear that the microbiome can have major influences on host biology, relatively little known about microbial communities in reproductive systems of males and females.The significant effects function fitness females, although these are rarely considered from an ecological or evolutionary perspective.Recent research indicates influence outcomes pre- postcopulatory sexual selection, as well generate conflict between sexes.Thus, complex coevolutionary dynamics emerge mating system microbiome, to shape patterns skew host, diversity across individuals species, ecology evolution microbes. Consequently, microbiomes also strong potential barriers populations. All multicellular organisms their bodies, biology. Most has focussed oral, skin, gut microbiomes, whereas microbiome. Here, we review empirical evidence show performance females. We then discuss likely repercussions for processes related selection conflict, isolation. argue knowledge fundamental our understanding strategies organisms. Animals plants live evolve a world dominated by microbes, bodies. A recent explosion host-associated (i.e., microbiota and/or see Glossary) revolutionising While earlier typically microorganisms pathological perspective, now widely accepted relationship microbes spans continuum, detrimental beneficial. Through health, physiology, development, behaviour [1Parfrey L.W. et al.Introduction: microbiome: pattern, process function.Mol. Ecol. 2018; 27: 1749-1765Crossref PubMed Scopus (5) Google Scholar,2Ezenwa V.O. al.Animal behavior microbiome.Science. 2012; 338: 198-199Crossref (194) Scholar], be seen integral part phenotype, potentially genome (e.g., hologenome concept [3Rosenberg E. Zilber-Rosenberg I. Microbes drive animals plants: concept.mBio. 2016; 7: e01395Crossref but [4Moran N.A. Sloan D.B. The concept: helpful hollow?.PLoS Biol. 2015; 13: e1002311Crossref Scholar]). considerable attention been paid role ecology, evolution, fitness, less (Box 1). This surprising given longstanding male female [5Rehewy M.S.E. al.Aerobic anaerobic bacterial flora semen fertile infertile groups men.Arch. Androl. 1979; 2: 263-268Crossref (0) Scholar]), most notably context sexually transmitted infections (STIs) [6Lockhart A.B. al.Sexually diseases animals: implications.Biol. Rev. 1996; 71: 415-471Crossref more DNA-sequencing studies demonstrating presence dynamic tissues [7Schoenmakers S. al.The matter microbiome.Obstet. Med. 2019; 12: 107-115Crossref (1) especially vagina [8Ravel J. al.Vaginal reproductive-age women.Proc. Natl. Acad. Sci. U. A. 2011; 108: 4680-4687Crossref (1227) Scholar,9Chen C. continuum along tract its relation uterine-related diseases.Nat. Commun. 2017; 8: 875Crossref Scholar]. Thus, represents outstanding challenge study communities.Box 1Defining Reproductive MicrobiomeIn broadest sense, defined operationally including bacteria, viruses unicellular algae, protozoans fungi, living any structure, organ, fluid, tissue makes contact with gametes (or gamete analogues, e.g., pollen gametophytes) organs another individual through mating, spawning, pollination. captures associated involved at point process, production release ejaculation) up fertilisation, tracts, gametes, fluids, genitalia, intromittent sperm transfer structures, pedipalps spiders, hectocotyli cephalopods, aedeagi insects, gonopods millipedes, claspers sharks rays, gonopodium Poeciliidae, hemipenes lizards snakes), spermatophores.This definition includes species into external environment, such fertilisers, wind- vector-pollinated angiosperms, fern spores released water, packages spermatophores) substrate uptake, where fertilisation mediated other pollination via animal vectors externally fertilising fish spawn within gills mussels, European bitterlings). In cases, reflects set which there members colonise opposite sex.While currently few this broad enables us develop arguments hypotheses generality. As structural functional refined definitions may begin emerge, narrower focus specialised biology different systems. Such might benefit identifying site human vaginal primates [11Yildirim al.Primate exhibit specificity without universal Lactobacillus dominance.ISME 2014; 2431-2444Crossref (50) copulatory spiders [108Spicer M.E. al.Spiders, sex: exposure alters funnel-web spiders.Ethology. 92: 91-99Google Scholar]).An important limited communities. Currently, generally unclear how established maintained, they processes. Furthermore, due prevalence mixing chance events (see Box 2) degree represent native assemblages transient, random assemblages, and, some instances, contribution range sources, environment genitalia) body sites host. many structure result both deterministic processes, lead spatiotemporal microbiomes. Consideration greater clarity future. spermatophores. sex. An Patterns variation studied interest mother–child transfer. humans, composition varies vagina, cervix, uterus, fallopian tubes, follicular fluid [9Chen Scholar,10Younes J.A. al.Women microbes: unexpected friendship.Trends Microbiol. 26: 16-32Abstract Full Text PDF Intriguingly, low-diversity bacteria genus whereas, mammals, lactobacilli constitute >1% Scholar, 12Swartz J.D. al.Characterization ewes cows reveals unique low levels near-neutral pH.Front. Vet. 1: 19Crossref 13Vrbanac murine perturbation pathogen group B Streptococcus.BMC 18: 197Crossref Several proposed explain uniqueness differences disease risk, diet [14Miller E.A. al.Lactobacilli dominance pH: why unique?.Front. 4-13Crossref (44) Scholar,15Stumpf R.M. primate comparative implications health disease.Am. Phys. Anthropol. 2013; 152: 119-134Crossref highly dynamic. For example, primates, changes age life-history phase, menstruation, pregnancy Intra- interindividual variability reported mice, factors influencing not oestrus cycling) [13Vrbanac These findings changed perception sterile environment. Less However, ejaculate taxa [16Poiani Complexity seminal fluid: review.Behav. Sociobiol. 2006; 60: 289-310Crossref (288) High-throughput sequencing shown ejaculates characterised biomass thus, requiring special care during sample collection processing avoid erroneous results [17Koedooder R. al.Identification evaluation tracts.Hum. Reprod. Update. 25: 298-325Crossref (4) diverse (greater richness) exhibits evenness than two do share taxa. described mice [18Javurek al.Discovery novel estrogen receptor alpha genetic status.Sci. Rep. 6: 23027Crossref (25) Scholar] penis [19Price L.B. circumcision microbiome.PLoS One. 2010; 5: e8422Crossref impact fertility impacts strategies, consider perspective 2), because full community assembly, succession, requires consideration interests occur plant kingdoms, indeed critical hosts, work date dioecious, reproducing internal fertilisation. Therefore, discussion taxa, will generality.Box 2Microbial Evolutionary Ecology MicrobiomeA modified metacommunity framework useful what shapes [109Miller E.T. al.Microbiomes metacommunities: ecology.Trends Evol. 33: 926-935Abstract Metacommunity assume local patch microbiome) shaped interactions immigration Immigration particularly shaping inevitable large scale often frequent, transmission mating. Mixing increase increasing rates increases multiple individuals, females males. Coupled fluctuating pressures imposed within-host physiological status, (and function) vary considerably time [88Gajer P. al.Temporal microbiota.Sci. Transl. 4: 132ra52Crossref (471) propensity extremely rapid dynamics, turn change [110Ellner S.P. al.Does matter? Measuring rate contemporary dynamics.Ecol. Lett. 14: 603-614Crossref (155) Scholar].Arguably, one compositionally 'holobiont hologenome' assumes (at least parts of) unit unlikely partners, acquiring environments, means vertically cotransmitted hence, create respect encounters.The affect co-vary genotype, key in, extent mate choice. From purely increased breakdown covariance. predictable covariance genotype genotype. rapidly adapt conditions (local adaptation; LA), host–microbe covariances. high migration genetically homogenise populations, reducing LA, resulting enhance LA adaptation [111Gandon al.Local gene-for-gene coevolution metapopulation model.Proc. Soc. B. 1997; 263: 1003-1009Google reinforced adaption co-occurring members, limit invasion foreign [112Tikhonov M. Community-level cohesion cooperation.eLife. 86Crossref (22) If certain roles determining (although yet know if case), microbe–host covariances implications.Microbial greatly affected events, further genotypes [113Sprockett D. al.Role priority early-life assembly microbiota.Nat. Gastroenterol. Hepatol. 15: 197-205Crossref (38) vaginal, regularly disturbed consequence enhancing importance [i.e., early (re)colonising species] [114Fukami T. Historical contingency assembly: integrating niches, pools, effects.Annu. Syst. 46: 1-23Crossref (338) Rapid (co)evolution populations divergent assemblies, stochasticity mutational reshape entire [115Gómez bacterium structuring natural community.Nat. 12453Crossref (21) Scholar].The phenotypic consequences mismatch even composition. First, equivalence weaken structure–function relationships [116Martiny J.B.H. light traits: phylogenetic perspective.Science. 350: aac9323Crossref (186) Second, ecosystems, strongly competitive [117Coyte K.Z. networks, competition, stability.Science. 663-666Crossref (354) interference exploitation temporally varying traits coevolution, pathogenesis reductions population size [118Inglis R.F. al.Spite versus cheats: competition among social virulence Pseudomonas aeruginosa.Evolution. 66: 3472-3484Crossref (13) Finally, selected response [119O'Brien al.Adaptation public goods cheats aeruginosa.Proc. 284: 20171089Crossref (10) directly hosts. Arguably, encounters. implications. Microbial

Language: Английский

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Experimental heatwaves negatively impact sperm quality in the zebra finch

Proceedings of the Royal Society B Biological Sciences, Journal Year: 2018, Volume and Issue: 285(1871), P. 20172547 - 20172547

Published: Jan. 17, 2018

For sexually reproducing species, functionally competent sperm are critical to reproduction. While high atmospheric temperatures known influence the timing of breeding, incubation and reproductive success in birds, effect temperature on quality remains largely unexplored. Here, we experimentally investigated impact ecologically relevant extreme cloacal morphology motility zebra finches Taeniopygia guttata . We periodically sampled males exposed 30°C or 40°C daily for 14 consecutive days. Following a 12-day (23°C) recovery period, birds were again heat, but under alternate treatment (e.g. initially 30°C). Elevated led an increase reduction proportion with normal morphology; these effects most notable conditions, influenced by duration heat exposure prior temperature. Our findings highlight potential role determining male fertility perhaps also constraining avian breeding. Given increased frequency heatwaves warming world, our results suggest need further work climatic influences fertility.

Language: Английский

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Sperm head morphology is associated with sperm swimming speed: A comparative study of songbirds using electron microscopy

Evolution, Journal Year: 2018, Volume and Issue: 72(9), P. 1918 - 1932

Published: July 17, 2018

Sperm exhibit extraordinary levels of morphological diversification across the animal kingdom. In songbirds, sperm have a helically shaped head incorporating distinct acrosomal membrane or "helical keel," form and extent which varies species. The functional significance this helical shape, however, remains unknown. Using scanning electron microscopy, we quantified inter‐ intraspecific variation in morphology 36 songbird species (Passeriformes: Passerida). phylogenetic comparative methods, investigated relationship between both swimming speed frequency extra‐pair young (EPY). We found that whose had relatively more pronounced (i.e., long acrosome, short nucleus, wide membrane, waveform along "core") faster‐swimming sperm. no evidence interspecific EPY, although did find among‐ within‐male traits were negatively correlated with EPY. Applying principles fluid mechanics, discuss how may influence speed, suggest further studies considering aspects beyond length are needed to improve our understanding structure‐function relationships.

Language: Английский

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Sperm performance in conspecific and heterospecific female fluid

Ecology and Evolution, Journal Year: 2016, Volume and Issue: 6(5), P. 1363 - 1377

Published: Jan. 30, 2016

Divergent sexual selection within allopatric populations may result in divergent phenotypes, which can act as reproductive barriers between upon secondary contact. This hypothesis has been most tested on traits involved precopulatory selection, with less work focusing that after copulation and before fertilization (i.e., postcopulatory prezygotic traits), particularly internally fertilizing vertebrates. However, species also drive trait divergence, resulting reduced performance of heterospecific sperm the female tract. Such incompatibilities, arising a by-product allopatry, represent barriers, analogous to species-assortative mating preferences. Here, we for three pairs taxa diverged phenotypes moderate-to-high opportunity (barn swallows Hirundo rustica versus sand martins Riparia riparia, two subspecies bluethroats, Luscinia svecica L. s. namnetum, great tits Parus major blue Cyanistes caeruleus). We swimming fluid from outer tract females, because greatest reduction number birds occurs swim across vagina. Contrary our expectations, swam equally well conspecific suggesting do not these taxon pairs, at this stage fertilization. therefore suggest divergence allopatry is insufficient cause widespread form impaired passerine birds.

Language: Английский

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Age-related changes in sperm traits and evidence for aging costs of sperm production in a sexually promiscuous passerine

Frontiers in Ecology and Evolution, Journal Year: 2023, Volume and Issue: 11

Published: Feb. 14, 2023

In many animal species, organismal performance declines with age in a process known as aging or senescence. Senescence typically leads to deterioration of physiological functionality and can impact the development primary sexual phenotypes. Sperm production is complex costly that sensitive changes individual state, yet remarkably little about age-related sperm costs production. Here we use non-linear generalized additive mixed models (GAMM) modelling evaluate postcopulatory traits European barn swallow ( Hirundo rustica ), relatively short lived sexually promiscuous passerine where male extra-pair fertilization success has been shown increase age. We confirmed positive relationship between midpiece length velocity this species. Within-male morphology were general absent, only decreasing linearly increasing age, although change was negligible compared overall variation size among males. contrast, cloacal protuberance (CP) changed nonlinearly an initial first third year life followed by plateau. The results further indicate existence trade-off investments survival males large CP tended have reduced lifespan. This seems consistent idea expensive associated post-copulatory

Language: Английский

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Subspecific variation in sperm morphology and performance in the Long-tailed Finch (Poephila acuticauda)

Avian Research, Journal Year: 2015, Volume and Issue: 6(1)

Published: Dec. 1, 2015

Evolutionary biology endeavours to explain biological diversity, and as such it is critical develop an understanding of the adaptive functional significance trait variation. Spermatozoa exhibit remarkable levels morphological diversification. However, our evolutionary causes this variation limited, especially at intraspecific level. We quantified in sperm morphology performance between two subspecies Long-tailed Finch (Poephila acuticauda P. a. hecki), a small grassfinch found tropical northern Australia. Despite zone secondary contact, these are maintained distinct forms: occurs western part species' range has yellow bill, while hecki exhibits red bill eastern range. small, but significant differences size (P. had longer narrower than which was surprising given recent origins taxa (i.e. 0.3 million years ago). Additionally, both exhibited high values between- within-male morphology, though case midpiece length significantly lower relative hecki. suggest observed result genetic drift reflect historical processes associated with divergence populations subspecies. Finally, we discuss potential implications findings for process population reproductive isolation.

Language: Английский

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Male age and its association with reproductive traits in captive and wild house sparrows

Journal of Evolutionary Biology, Journal Year: 2019, Volume and Issue: 32(12), P. 1432 - 1443

Published: Sept. 17, 2019

Abstract Evolutionary theory predicts that females seek extra‐pair fertilizations from high‐quality males. In socially monogamous bird species, it is often old males are most successful in fertilizations. Adaptive models of female mate choice suggest may produce offspring higher genetic quality than young because they have proven their survivability. However, also more likely to show signs reproductive senescence, such as reduced sperm quality. To better understand why account for a disproportionally large number and what the consequences mating with are, we compared several traits both captive wild house sparrows, Passer domesticus . Sperm morphological cloacal protuberance volume (a proxy load) did not differ substantially. delivered almost three times female's egg We discuss possibility post‐copulatory advantage over mated

Language: Английский

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The effects of male social environment on sperm phenotype and genome integrity

Journal of Evolutionary Biology, Journal Year: 2019, Volume and Issue: 32(6), P. 535 - 544

Published: Feb. 28, 2019

Sperm function and quality are primary determinants of male reproductive performance hence fitness. The presence rival males has been shown to affect ejaculate sperm traits in a wide range taxa. However, physiological conditions may not only phenotypic but also their genetic epigenetic signatures, affecting the fitness resulting offspring. We investigated effects male-male competition on using TUNEL assays geometric morphometrics zebrafish, Danio rerio. found that produced by exposed high had smaller heads larger midpiece flagellum than under low competition. Head flagella appeared less sensitive osmotic stress induced activation with water. In addition, more showed signals DNA damage ejaculates These findings suggest have positive negative integrity. Overall, facing produce faster swimming competitive this come at cost for next generation.

Language: Английский

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Sperm divergence in a passerine contact zone: Indication of reinforcement at the gametic level

Evolution, Journal Year: 2018, Volume and Issue: 73(2), P. 202 - 213

Published: Dec. 31, 2018

Postcopulatory sexual selection may promote evolutionary diversification in sperm form, but the contribution of between‐species divergence morphology to origin reproductive isolation and speciation remains little understood. To assess possible role isolation, we studied two closely related bird species, common nightingale (Luscinia megarhynchos) thrush luscinia), that hybridize a secondary contact zone spanning Central Eastern Europe. We found: (1) striking between species total length, accompanied by difference length mitochondrial component; (2) greater sympatry than allopatry, with evidence for character displacement head detected L. megarhynchos; (3) interspecific hybrids showing intermediate parental no decreased quality (the proportion abnormal spermatozoa ejaculates). Our results demonstrate does not result intrinsic postzygotic contribute postcopulatory prezygotic isolation. This could be strengthened reinforcement.

Language: Английский

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Variation in sperm morphology and performance in tree sparrow (Passer montanus) under long-term environmental heavy metal pollution

Ecotoxicology and Environmental Safety, Journal Year: 2020, Volume and Issue: 197, P. 110622 - 110622

Published: April 17, 2020

Language: Английский

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