2024
Systematic approaches to assessing high temperature limits to fertility in animals
Bretman A, Fricke C, Baur J, Berger D, Breedveld MC, Dierick D, Canal Domenech B, Drobniak SM, Ellers J, English S, Gasparini C, Iossa G, Lagisz M, Nakagawa S, Noble DWA, Pottier P, Ramm SA, Rowe M, Schultner E, Schou M, Simões P, Stockley P, Vasudeva R, Weaving H, Price TAR, SnookRR (2024)
Journal of Evolutionary Biology, in press. DOI: 10.1093/jeb/voae021
We set out an experimental framework for measuring thermal fertility limits (TFLs) and the thermal sensitivity of fertility (TSF), and discuss how it can be implemented across diverse animal groups.
A systematic map of studies testing the relationship between temperature and animal reproduction.
Dougherty L, Frost F, Maenpaa M, Rowe M, Cole B, Vasudeva R, Pottier P, Schultner E, Macartney E, Lindenbaum I, Smith J, Carazo P, Graziano M, Weaving H, Canal Domenech B, Berger D, Meena A, Bishop T, Noble D, Simões P, Baur J, Breedveld M, Svensson E, Lancaster L, Ellers J, De Nardo A, Santos M, Ramm SA, Drobniak S, Redana M, Tuni C, Pilakouta N, Zizzari ZV, Iossa G, Lüpold S, Koppik M, Early R, Gasparini C, Nakagawa S, Lagisz M, Bretman A, Fricke C, Snook R, Price T (2024)
Ecological Solutions and Evidence 5:e12303. DOI: 10.1002/2688-8319.12303
The first major output from our ESEB-funded Special Topic Network on the Evolutionary Ecology of Thermal Fertility Limits, we provide a systematic map of the huge literature linking temperature to reproductive outcomes.
Sex-limited experimental evolution drives transcriptomic divergence in a hermaphrodite
Cīrulis A, Nordén AK, Churcher AM, Ramm SA, Zadesenets KS, Abbott JK
Genome Biology & Evolution, in press. DOI: 10.1093/gbe/evad235Following sex-limited selection to simulate the early stages of sex chromosome evolution, we document transcriptomic responses in a broad suite of genes, with evidence of a prominent role for divergence in testis-limited transcript expression.
2023
Rapid evolution of sex role specialization in a hermaphrodite under sex-limited selection
Nordén AK, Ramm SA, Abbott JK
Evolution, in press. DOI: 10.1093/evolut/qpad025To simulate the early stages of sex chromosome evolution, we use experimentally evolving lines constrained to reproduce only through the male or the female sex function to demonstrate rapid divergence in sex-specific fitness consistent with sex role specialization.
Timeless or tainted? The effects of male ageing on seminal fluid
Fricke C, Sanghvi K, Emery M, Lindenbaum I, Wigby S, Ramm SA & Sepil I (2023)
Frontiers in Ecology & Evolution, in press. DOI: 10.3389/fevo.2023.1066022 Our contribution to the Research Topic The Evolutionary Roots of Reproductive Ageing and Reproductive Health Across the Tree of Life, we reports a systematic review of ageing effects on seminal fluid and set out a research agenda to understand how seminal fluid-mediated effects contribute to male reproductive ageing.
2022
Waiting for love but not forever: modelling the evolution of waiting time to selfing in hermaphrodites
Blüml C, Ramm SA, van Benthem KJ, Wittmann MJ (2022)
Frontiers in Ecology & Evolution 10:1002475. DOI: 10.3389/fevo.2022.1002475
We model the evolution of waiting times to explore how delayed selfing evolves in response to density and density fluctuations.
2021
The baculum affects paternity success of first but not second males in house mouse sperm competition
Winkler L, Lindholm AK, Ramm SA, Sutter A (2021)
BMC Ecology & Evolution 21:159. DOI: 10.1186/s12862-021-01887-6
We report experimental evidence linking baculum width to fertilisation success, suggesting that baculum-mediated stimulation is advantageous in sperm competition.
2020
Material heterogeneity of male genitalia reduces genital damage in a bushcricket during sperm removal behaviour
Matsumura Y, Jafarpour M, Ramm SA, Reinhold K, Gorb SN, Rajabi H (2020)
The Science of Nature 107: 52. DOI: 10.1007/s00114-020-01706-w
We use micro-CT and confocal LSM to study the functional morphology of genital interactions in the bushcricket Metaplastes ornatus, revealing evidence of adaptations to sperm removal behaviour.
Seminal fluid and accessory male investment in sperm competition
Ramm SA (2020)
Philosophical Transactions of the Royal Society B 375: 20200068. DOI: 10.1098/rstb.2020.0068
As my contribution to celebrating ‘Fifty Years of Sperm Competition’, I review evidence for the differential production and allocation of seminal fluid under sperm competition, and ask how sperm and seminal fluid investment strategies covary.
The hidden ageing costs of sperm competition
Lemaitre J-F, Gaillard J-M, Ramm SA (2020)
Ecology Letters, in press. DOI: 10.1111/ele.13593
We set out a series of hypotheses about how male investment in traits linked to sperm competition ultimately impacts both reproductive and actuarial senescence.
Divergence of seminal fluid gene expression and function among natural snail populations
Nakadera Y, Thornton Smith A, Daupagne L, Coutellec MA, Koene JM, Ramm SA (2020)
Journal of Evolutionary Biology, in press. DOI: 10.1111/jeb.13683
We uncover evidence for the rapid evolution of both seminal fluid expression and the strength of post-mating responses by mating partners induced by seminal fluid.
Disentangling a shared trait: male control over mate guarding duration revealed by a mate exchange experiment
Haneke-Reinders M, Mazur AP, Zyma O, Ramm SA, Reinhold K (2020)
Behavioral Ecology & Sociobiology 74:54. DOI: 10.1007/s00265-020-02832-1
We show in the cricket Gryllodes sigillatus that males seem to determine the duration of the mate guarding phase, and invest more in guarding heavier females.
Evidence for inter-population variation in waiting times in a self-fertilizing flatworm
Giannakara A, Ramm SA (2020)
Invertebrate Reproduction and Development, in press. DOI: 10.1080/07924259.2020.1732485
We report that Macrostomum hystrix individuals from two natural populations readily self when isolated, despite substantial inbreeding depression and in contrast to a previously studied population.
The free-living flatworm Macrostomum lignano
Wudarski J, Egger B, Ramm SA, Schärer L, Ladurner P, Zadasenets KS, Rubtsov NB, Mouton S, Berezikov E (2020)
EvoDevo 11:5. DOI: 10.1186/s13227-020-00150-1
A short primer on Macrostomum biology, the first for a series in EvoDevo on emerging experimental systems.
Effects of two seminal fluid proteins on post-mating behavior in the simultaneously hermaphroditic flatworm Macrostomum lignano
Weber M, Patlar B, Ramm SA (2020)
Journal of Evolutionary Biology, in press. DOI: 10.1111/jeb.13606
Using a targeted RNAi approach, we identify a seminal fluid protein that stimulates the post-copulatory ‘suck behaviour’ of mating partners in Macrostomum lignano.
Genotype-by-environment interactions for seminal fluid expression and sperm competitive ability
Patlar B, Weber M, Ramm SA (2020)
Journal of Evolutionary Biology 33:225-236. DOI: 10.1111/jeb.13568
We demonstrate that expression of one of our newly discovered ‘suckless’ transcripts depends on GEIs, and that this may be linked to sperm competition outcomes.
Seminal fluid-mediated manipulation of post-mating behavior in a simultaneous hermaphrodite
Patlar B, Weber M, Temizyürek T, Ramm SA (2020)
Current Biology 30:143-149. DOI: 10.1016/j.cub.2019.11.018
We use a combination of quantitative genetics and RNAi to identify two seminal fluid proteins that suppress the ‘suck’ behaviour of mating partners, mediating sexual conflict over ejaculate fate.
2019
Seminal fluid-mediated fitness effects in the simultaneously hermaphroditic flatworm Macrostomum lignano
Weber M, Giannakara A, Ramm SA (2019)
Ecology and Evolution 9:13889-13901. DOI: 10.1002/ece3.5825
We report an RNAi screen to identify candidate seminal fluid proteins affecting fertility and sperm competitive ability.
Impact of low sperm competition on male reproductive trait allometries in a bushcricket
Winkler L, ML Kirch, Reinhold K, Ramm SA (2019)
BMC Evolutionary Biology 19:185. DOI: 10.1186/s12862-019-1514-0
We examine how the evolution of sperm removal behaviour by males might have affected testis, spermatophore gland and genital allometry in Metaplastes ornatus.
Sex allocation plasticity on a transcriptome scale: socially-sensitive gene expression in a simultaneous hermaphrodite
Ramm SA, Lengerer B, Arbore R, Pjeta R, Wunderer J, Giannakara A, Berezikov E, Ladurner P, Schärer L (2019)
Molecular Ecology 28:2321-2341. DOI: 10.1111/mec.15077
Using a combination of RNASeq, in situ hybridization and RNAi, we demonstrate the wholesale changes in reproductive gene expression underlying sex allocation plasticity in Macrostomum lignano.
Plastic expression of seminal fluid protein genes in a simultaneously hermaphroditic snail
Nakadera Y, Giannakara A, Ramm SA (2019)
Behavioral Ecology 30:904-913. DOI: 10.1093/beheco/arz027
We demonstrate plasticity in the expression of several seminal fluid genes in response to the availability of mates, but no evidence for differential expression according to sperm competition intensity.
Genetic and environmental variation in transcriptional expression of seminal fluid proteins
Patlar B, Weber M, Ramm SA (2019)
Heredity 122:595-611. DOI: 10.1038/s41437-018-0160-4
We describe the tightly integrated nature of the seminal fluid transcriptome to establish the quantitative genetic basis of seminal fluid investment and composition.
2018
Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal
Winkler L, Ramm SA (2018)
Biology Letters 14:20180570. DOI: 10.1098/rsbl.2018.0570
We demonstrate phenotypic plasticity in sperm production in the preferentially outcrossing flatworm Macrostomum hystrix, with individuals conserving investment under enforced selfing.
A targeted in situ hybridization screen identifies putative seminal fluid proteins in a simultaneously hermaphroditic flatworm
Weber M, Lengerer B, Pjeta R, Wunderer J, Rodrigues M, Schärer L, Ladurner P, Ramm SA (2018)
BMC Evolutionary Biology 124:32-40. DOI: 10.1186/s12862-018-1187-0
We provide an extensive catalogue of putative seminal fluid proteins in Macrostomum lignano, based on determining their prostate-specific gene expression.
Divergent testis allometry in two subspecies of the bushcricket Poecilimon veluchianus
Koschmieder M, Müller M, Reinhold K, Ramm SA (2018)
Biological Journal of the Linnean Society 124:32-40. DOI: 10.1093/biolinnean/bly018
We find that two bushcricket sub-species both exhibit positive testis allometry, but differ markedly in the allometric intercept.
The evolution of gonad expenditure and gonadosomatic index (GSI) in male and female broadcast-spawning invertebrates
Parker GA, Ramm SA, Lehtonen J, Henshaw JM (2018)
Biological Reviews. DOI: 10.1111/brv.12363
A comparative and theoretical investigation of sex-specific GSI patterns in broadcast spawners.
2017
Promiscuity punishes sexual deviants (Perspective)
Engqvist L, Ramm SA (2017)
Molecular Ecology 26:5359-5361. DOI: 10.1111/mec.14355
A commentary on this paper showing that multiple mating by female mice provides some protection against the spread of a selfish genetic element.
Strategic investment in sperm removal behaviour in a bushcricket
Foraita M, Lehfeldt S, Reinhold K, Ramm SA (2017)
Journal of Insect Behavior. DOI: 10.1007/s10905-017-9608-2
We investigate variation in this intriguing sperm removal behaviour in the bushcricket Metaplastes ornatus, finding that males conserve investment when paired with unmated females.
Self-fertilization, sex allocation and spermatogenesis kinetics in the hypodermically-inseminating flatworm Macrostomum pusillum
Giannakara A, Ramm SA (2017)
Journal of Experimental Biology. DOI: 10.1242/jeb.149682
We demonstrate the ability of M. pusillum to self-fertilize, and present a series of findings suggesting that this is a frequent and maybe even the preferred reproductive mode of this species.
Exploring the sexual diversity of flatworms: ecology, evolution and the molecular biology of reproduction
Ramm SA (2017)
Molecular Reproduction & Development. DOI: 10.1002/mrd.22669
I review various “lifestyle choices” made by flatworms, such as whether to be free-living or parasitic; to reproduce sexually or asexually; to be separate-sexed or hermaphroditic; and if the latter, whether to outcross or self-fertilise as well as how to optimise sex allocation.
2016
Experimentally evolved and phenotypically plastic responses to enforced monogamy in a hermaphroditic flatworm
Janicke T, Sandner P, Ramm SA, Vizoso DB, Schärer L (2016)
Journal of Evolutionary Biology. DOI: 10.1111/jeb.12910
Based on 32 selection lines evolving for 20 generations, we show that many sexual traits did not diverge under different mating regimes, but continued to exhibit substantial phenotypic plasticity.
Sperm competition-induced plasticity in the speed of spermatogenesis
Giannakara A, Schärer L, Ramm SA (2016)
BMC Evolutionary Biology 16: 60. DOI: 10.1186/s12862-016-0629-9
The first experimental evidence for adaptive plasticity in spermatogenesis speed: worms raised under more competitive conditions not only make more sperm, but make each one faster.
Integrating perspectives on rodent sperm competition
Ramm SA, Stockley P (2016)
Advances in the Study of Behavior 48. DOI: 10.1016/bs.asb.2016.02.003
An in-depth review of male adaptations to sperm competition in this model vertebrate group, including studies of copulatory behaviour, sperm production and allocation, seminal fluid and genitalia.
Hermaphrodites
Schärer L, Ramm SA (2016)
Chapter 160 in Encyclopedia of Evolutionary Biology (R. Kliman, ed.). Academic Press.
DOI: 10.1016/B978-0-12-800049-6.00160-8
A primer on evolutionary thinking about sex in both simultaneous and sequential hermaphrodites.
2015
Sperm competition risk drives plasticity in seminal fluid composition
Ramm SA, Edward DA, Claydon AJ, Hammond DE, Brownridge P, Hurst JL, Beynon RJ, Stockley P (2015)
BMC Biology 13: 87. DOI: 10.1186/s12915-015-0197-2
Using proteomics methods, we reveal how male mice adjust seminal fluid protein production in response to social environmental cues.
Male birch catkin bugs vary copula duration to invest more in matings with novel females
Reinhold K, Engqvist L, Consul A, Ramm SA (2015)
Animal Behaviour 109: 161–166 DOI: 10.1016/j.anbehav.2015.08.020
We report a series of experiments that collectively imply strategic allocation of mating effort my male birch catkin bugs, in favour of novel females.
Hypodermic self-insemination as a reproductive assurance strategy
Ramm SA, Schlatter A, Poirier M, Schärer L (2015)
Proceedings of The Royal Society B Biological Sciences 282: 20150660. DOI: 10.1098/rspb.2015.0660
Experimental evidence that Macrostomum hystrix flatworms use a striking mechanism of self-injecting sperm into their own body in order to self-fertilise their eggs.
Making the complex simple: a comment on Valcu and Kempenaers (Invited Commentary)
Ramm SA (2015)
Behavioral Ecology 26: 16. DOI: 10.1093/beheco/aru167
A commentary to accompany the publication of Valcu and Kempenaers’ Invited Review on “Proteomics in behavioral ecology“
2014
Sperm competition and the evolution of reproductive systems (Editorial)
Ramm SA (2014)
Molecular Human Reproduction 20(12): 1159–1160. DOI: 10.1093/molehr/gau076
Introduction to a special issue of MHR presenting four reviews on various topics linked to sperm competition.
Sperm competition and the evolution of spermatogenesis
Ramm SA, Schärer L, Ehmcke J, Wistuba J (2014)
Molecular Human Reproduction 20(12): 1169–1179. DOI: 10.1093/molehr/gau070
This review focuses on how sperm competition has been a crucial selection pressure shaping various aspects of spermatogenesis.
Sexual conflict in hermaphrodites
Schärer L, Janicke T, Ramm SA (2014)
Cold Spring Harbor Perspectives in Biology. DOI: 10.1101/cshperspect.a017673
We review how sexual conflict concepts can be applied to hermaphrodites. Also included as one chapter in: Rice WR & Gavrilets S (eds.) The Genetics and Biology of Sexual Conflict. Cold Spring Harbor Laboratory Press.
Sequential male mate choice under sperm competition risk
Ramm SA, Stockley P (2014)
Behavioral Ecology 25 (3): 660–667. DOI: 10.1093/beheco/aru037
Male house mice can be coy too, targeting their reproductive effort towards the most favourable mating opportunities.
The evolutionary ecology of testicular function: size isn’t everything
Ramm SA, Schärer L (2014)
Biological Reviews 89: 874-888. DOI: 10.1111/brv.12084
We review ways in which post-mating sexual selection influences spermatogenesis and testicular function besides via gross testis size.
2013
Comment on “Bateman in Nature: Predation on Offspring Reduces the Potential for Sexual Selection”
Ramm SA, Jonker R, Reinhold K, Szekely T, Trillmich F, Schmoll T, Schielzeth H, Freckleton RP (2013)
Science 340(6132): 549. DOI: 10.1126/science.1233298
A Technical Comment on the application of Bateman gradient analyses to field data.
Baculum morphology predicts reproductive success of male house mice under sexual selection
Stockley P, Ramm SA, Sherborne AL, Thom MDF, Paterson S, Hurst JL (2013)
BMC Biology 11(1): 66. DOI: 10.1186/1741-7007-11-66
First experimental evidence in a mammal that genitalia influence male reproductive success.
Male control of sperm transfer dynamics in a spermatophore-donating bushcricket
Reinhold K, Ramm SA (2013)
Behavioral Ecology and Sociobiology 67(3): 395–398. DOI: 10.1007/s00265-012-1459-4
A reciprocal cross experiment between males and females from two subspecies suggests sperm uptake from the spermatophore is a male-determined trait.
2012
Occurrence, costs and heritability of delayed selfing in a free-living flatworm
Ramm SA, Vizoso DB, Schärer L (2012)
Journal of Evolutionary Biology 25(12): 2559–2568. DOI: 10.1111/jeb.12012
Macrostomum hystrix exhibits delayed selfing behaviour, a reproductive assurance mechanism in the absence of outcrossing opportunities.
Sperm competition roles and ejaculate investment in a promiscuous mammal
Lemaître JF, Ramm SA, Hurst JL, Stockley P (2012)
Journal of Evolutionary Biology 25(6): 1216–1225. DOI: 10.1111/j.1420-9101.2012.02511.x
Contrary to predictions from theory, dominant male bank voles appear competitively superior to subordinates in various post-copulatory traits.
Heterogenous turnover of sperm and seminal vesicle proteins in the mouse revealed by dynamic metabolic labelling
Claydon A, Ramm SA, Penningon A, Hurst JL, Stockley P, Beynon RJ (2012)
Molecular & Cellular Proteomics 11(6): M111.014993. DOI: 10.1074/mcp.m111.014993
We use proteomics techniques to demonstrate the rapid turnover of seminal fluid proteins.
Inbreeding avoidance behaviour of male bank voles in relation to social status
Lemaitre J-F, Ramm SA, Hurst JL, Stockley P (2012)
Animal Behaviour 83(2): 453–457. DOI: 10.1016/j.anbehav.2011.11.017
Male preference for nonsibling females does not vary with social status in male bank voles.
Genital morphology linked to social status in the bank vole (Myodes glareolus)
Lemaitre J-F, Ramm SA, Jennings N, Stockley P (2012)
Behavioral Ecology and Sociobiology 66(1): 97–105. DOI: 10.1007/s00265-011-1257-4
Dominant male bank voles have wider bacula than subordinates, and baculum width exhibits positive allometry.
2011
Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal
Lemaitre J-F, Ramm SA, Hurst JL, Stockley P (2011)
Proceedings of The Royal Society B Biological Sciences 278(1709): 1171–1176. DOI: 10.1098/rspb.2010.1828
The first experimental evidence that sperm competition cues affect male investment in seminal fluid production.
2010
Sperm competition and sperm length influence the rate of mammalian spermatogenesis
Ramm SA, Stockley P (2010)
Biology Letters 6(2): 219–221. DOI: 10.1098/rsbl.2009.0635
A comparative study finds that sperm competition and sperm length have significant and opposing effects on the duration of spermatogenesis.
Sexual selection and the rodent baculum: an intraspecific study in the house mouse (Mus musculus domesticus)
Ramm SA, Khoo L, Stockley P (2010)
Genetica 138(1): 129–137. DOI: 10.1007/s10709-009-9385-8
As part of a special issue, we test various indirect predictions of the sexual selection hypothesis for genital evolution.
2009
Sperm competition and brain size evolution in mammals
Lemaitre J-F, Ramm SA, Barton RA, Stockley P (2009)
Journal of Evolutionary Biology 22(11): 2215–2221. DOI: 10.1111/j.1420-9101.2009.01837.x
A negative correlation between brain size and testis size in bats appears not to be a general pattern in other mammals.
Male house mice do not adjust sperm allocation in response to odours from related or unrelated rivals
Ramm SA, Stockley P (2009)
Animal Behaviour 78(3): 685–690. DOI: 10.1016/j.anbehav.2009.06.018
Odour cues from related or unrelated rivals appear not to influence immediate sperm allocation decisions.
Adaptive plasticity of mammalian sperm production in response to social experience
Ramm SA, Stockley P (2009)
Proceedings of The Royal Society B Biological Sciences 276(1657): 745–751. DOI: 10.1098/rspb.2008.1296
We provide the first experimental evidence in a vertebrate that males use sperm competition cues to modify sperm production.
Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition
Ramm SA, McDonald L, Hurst JL, Beynon RJ, Stockley P (2009)
Molecular Biology and Evolution 26(1): 189–198. DOI: 10.1093/molbev/msn237
We show that rodent seminal fluid proteomes are hugely diverse across species, with variation in one key protein linked to sperm competition.
2008
Sexual selection and the adaptive evolution of mammalian ejaculate proteins
Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD (2008)
Molecular Biology and Evolution 25(1): 207–219. DOI: 10.1093/molbev/msm242
Evidence for the rapid evolution of reproductive genes and tests for associations with variation in sperm competition levels.
Encoding choosiness: female attraction requires prior physical contact with individual male scents in mice
Ramm SA, Cheetham SA, Hurst JL (2008)
Proceedings of The Royal Society B Biological Sciences 275(1644): 1727–1735. DOI: 10.1098/rspb.2008.0302
We show that female mice are only attracted to airborne urinary volatiles from males whose urine they have previously contacted, implying individual recognition.
2007
Sexual selection and genital evolution in mammals: A phylogenetic analysis of baculum length
Ramm SA (2007)
The American Naturalist 169(3): 360–369. DOI: 10.1086/510688
Comparative evidence that genitalia are under sexual selection in mammals.
Ejaculate allocation under varying sperm competition risk in the house mouse, Mus musculus domesticus
Ramm SA, Stockley P (2007)
Behavioral Ecology 18(2): 491–495. DOI: 10.1093/beheco/arm003
Males surprisingly allocate fewer sperm under conditions simulating an elevated risk of sperm competition, likely due to a correlated response in mating behaviour.
2005
Sperm competition and the evolution of male reproductive anatomy in rodents
Ramm SA, Parker GA, Stockley P (2005)
Proceedings of The Royal Society B Biological Sciences 272(1566): 949–955. DOI: 10.1098/rspb.2004.3048
We find that multiple paternity levels predict relative testis size, and demonstrate correlated evolution of male investment in sperm and seminal fluid production.
the ramm lab 