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Bayram, H. L., Sayadi, A., Immonen, E. & Arnqvist, G. (2019). Identification of novel ejaculate proteins in a seed beetle and division of labour across male accessory reproductive glands. Insect biochemistry and molecular biology, 104, 50-57
Open this publication in new window or tab >>Identification of novel ejaculate proteins in a seed beetle and division of labour across male accessory reproductive glands
2019 (English)In: Insect biochemistry and molecular biology, ISSN 0965-1748, Vol. 104, p. 50-57Article in journal (Refereed) Published
Abstract [en]

The male ejaculate contains a multitude of seminal fluid proteins (SFPs), many of which are key reproductive molecules, as well as sperm. However, the identification of SFPs is notoriously difficult and a detailed understanding of this complex phenotype has only been achieved in a few model species. We employed a recently developed proteomic method involving whole-organism stable isotope labelling coupled with proteomic and transcriptomic analyses to characterize ejaculate proteins in the seed beetle Callosobruchus maculatus. We identified 317 proteins that were transferred to females at mating, and a great majority of these showed signals of secretion and were highly male-biased in expression in the abdomen. These male-derived proteins were enriched with proteins involved in general metabolic and catabolic processes but also with proteolytic enzymes and proteins involved in protection against oxidative stress. Thirty-seven proteins showed significant homology with SFPs previously identified in other insects. However, no less than 92 C. maculatus ejaculate proteins were entirely novel, receiving no significant blast hits and lacking homologs in extant data bases, consistent with a rapid and divergent evolution of SFPs. We used 3D micro-tomography in conjunction with proteomic methods to identify 5 distinct pairs of male accessory reproductive glands and to show that certain ejaculate proteins were only recovered in certain male glands. Finally, we provide a tentative list of 231 candidate female-derived reproductive proteins, some of which are likely important in ejaculate processing and/or sperm storage.

Place, publisher, year, edition, pages
Pergamon, 2019
Keywords
Reproductive proteins, Stable isotope labelling, Acps, Sperm competition, Seminal fluid
National Category
Biochemistry and Molecular Biology Zoology
Identifiers
urn:nbn:se:uu:diva-373579 (URN)10.1016/j.ibmb.2018.12.002 (DOI)000458938500006 ()30529580 (PubMedID)
Funder
Swedish Research Council, 621-2014-4523Knut and Alice Wallenberg FoundationEU, European Research Council, GENCON AdG-294333
Available from: 2019-01-15 Created: 2019-01-15 Last updated: 2019-03-11Bibliographically approved
Sayadi, A., Martínez Barrio, Á., Immonen, E., Dainat, J., Berger, D., Tellgren-Roth, C., . . . Arnqvist, G. (2019). The genomic footprint of sexual conflict. Nature Ecology & Evolution, 3(12), 1725-1730
Open this publication in new window or tab >>The genomic footprint of sexual conflict
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2019 (English)In: Nature Ecology & Evolution, E-ISSN 2397-334X, Vol. 3, no 12, p. 1725-1730Article in journal (Refereed) Published
Abstract [en]

Genes with sex-biased expression show a number of unique properties and this has been seen as evidence for conflicting selection pressures in males and females, forming a genetic 'tug-of-war' between the sexes. However, we lack studies of taxa where an understanding of conflicting phenotypic selection in the sexes has been linked with studies of genomic signatures of sexual conflict. Here, we provide such a link. We used an insect where sexual conflict is unusually well understood, the seed beetle Callosobruchus maculatus, to test for molecular genetic signals of sexual conflict across genes with varying degrees of sex-bias in expression. We sequenced, assembled and annotated its genome and performed population resequencing of three divergent populations. Sex-biased genes showed increased levels of genetic diversity and bore a remarkably clear footprint of relaxed purifying selection. Yet, segregating genetic variation was also affected by balancing selection in weakly female-biased genes, while male-biased genes showed signs of overall purifying selection. Female-biased genes contributed disproportionally to shared polymorphism across populations, while male-biased genes, male seminal fluid protein genes and sex-linked genes did not. Genes showing genomic signatures consistent with sexual conflict generally matched life-history phenotypes known to experience sexually antagonistic selection in this species. Our results highlight metabolic and reproductive processes, confirming the key role of general life-history traits in sexual conflict.

Place, publisher, year, edition, pages
Nature Publishing Group, 2019
National Category
Genetics Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-402373 (URN)10.1038/s41559-019-1041-9 (DOI)000500728800022 ()31740847 (PubMedID)
Funder
Swedish Research CouncilKnut and Alice Wallenberg FoundationEU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2014-4523Swedish Research Council Formas, 2018-00705
Available from: 2020-02-03 Created: 2020-02-03 Last updated: 2020-02-03Bibliographically approved
Hämäläinen, A., Immonen, E., Tarka, M. & Schuett, W. (2018). Evolution of sex-specific pace-of-life syndromes: causes and consequences. Behavioral Ecology and Sociobiology, 72(3), Article ID UNSP 50.
Open this publication in new window or tab >>Evolution of sex-specific pace-of-life syndromes: causes and consequences
2018 (English)In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 72, no 3, article id UNSP 50Article, review/survey (Refereed) Published
Abstract [en]

Males and females commonly differ in their life history optima and, consequently, in the optimal expression of life history, behavioral and physiological traits involved in pace-of-life syndromes (POLS). Sex differences in mean trait expression typically result if males and females exhibit different fitness optima along the same pace-of-life continuum, but the syndrome structure may also differ for the sexes. Due to sex-specific selective pressures imposed by reproductive roles and breeding strategies, the sexes may come to differ in the strength of correlation among traits, or different traits may covary in males and females. Ignorance of these selective forces operating between and within the sexes may lead to flawed conclusions about POLS manifestation in the species, and stand in the way of understanding the evolution, maintenance, and variability of POLS. We outline ways in which natural and sexual selection influence sex-specific trait evolution, and describe potential ultimate mechanisms underlying sex-specific POLS. We make predictions on how reproductive roles and the underlying sexual conflict lead to sex-specific trait covariances. These predictions lead us to conclude that sexual dimorphism in POLS is expected to be highly prevalent, allow us to assess possible consequences for POLS evolution, and provide guidelines for future studies.

Keywords
Integrated phenotype, Life history, Mating system, Personality, POLS, Sexual dimorphism
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-357038 (URN)10.1007/s00265-018-2466-x (DOI)000428864200023 ()
Funder
EU, European Research Council, AdG-294333The Research Council of Norway, SFF-III 223257
Available from: 2018-08-10 Created: 2018-08-10 Last updated: 2018-08-10Bibliographically approved
Immonen, E., Hämäläinen, A., Schuett, W. & Tarka, M. (2018). Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms. Behavioral Ecology and Sociobiology, 72(3), Article ID UNSP 60.
Open this publication in new window or tab >>Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms
2018 (English)In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 72, no 3, article id UNSP 60Article, review/survey (Refereed) Published
Abstract [en]

Sex differences in life history, physiology, and behavior are nearly ubiquitous across taxa, owing to sex-specific selection that arises from different reproductive strategies of the sexes. The pace-of-life syndrome (POLS) hypothesis predicts that most variation in such traits among individuals, populations, and species falls along a slow-fast pace-of-life continuum. As a result of their different reproductive roles and environment, the sexes also commonly differ in pace-of-life, with important consequences for the evolution of POLS. Here, we outline mechanisms for how males and females can evolve differences in POLS traits and in how such traits can covary differently despite constraints resulting from a shared genome. We review the current knowledge of the genetic basis of POLS traits and suggest candidate genes and pathways for future studies. Pleiotropic effects may govern many of the genetic correlations, but little is still known about the mechanisms involved in trade-offs between current and future reproduction and their integration with behavioral variation. We highlight the importance of metabolic and hormonal pathways in mediating sex differences in POLS traits; however, there is still a shortage of studies that test for sex specificity in molecular effects and their evolutionary causes. Considering whether and how sexual dimorphism evolves in POLS traits provides a more holistic framework to understand how behavioral variation is integrated with life histories and physiology, and we call for studies that focus on examining the sex-specific genetic architecture of this integration.

Keywords
Sexual conflict, Sexual dimorphism, Genetic architecture, Personality, Life history evolution, Physiology
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-357039 (URN)10.1007/s00265-018-2462-1 (DOI)000428864200019 ()29576676 (PubMedID)
Funder
EU, European Research Council, AdG-294333
Available from: 2018-08-10 Created: 2018-08-10 Last updated: 2018-08-10Bibliographically approved
Immonen, E., Sayadi, A., Bayram, H. & Arnqvist, G. (2017). Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus. Genome Biology and Evolution, 9(3), 677-699
Open this publication in new window or tab >>Mating Changes Sexually Dimorphic Gene Expression in the Seed Beetle Callosobruchus maculatus
2017 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 9, no 3, p. 677-699Article in journal (Refereed) Published
Abstract [en]

Sexually dimorphic phenotypes arise largely from sex-specific gene expression, which hasmainly been characterized in sexually naive adults. However, we expect sexual dimorphism in transcription to be dynamic and dependent on factors such as reproductive status. Mating induces many behavioral and physiological changes distinct to each sex and is therefore expected to activate regulatory changes in many sex-biased genes. Here, we first characterized sexual dimorphism in gene expression in Callosobruchus maculatus seed beetles. We then examined how females and males respond to mating and how it affects sex-biased expression, both in sex-limited (abdomen) and sex-shared (head and thorax) tissues. Mating responses were largely sex-specific and, as expected, females showed more genes responding compared with males (similar to 2,000 vs. similar to 300 genes in the abdomen, similar to 500 vs. similar to 400 in the head and thorax, respectively). Of the sex-biased genes present in virgins, 16%(1,041 genes) in the abdomen and 17%(243 genes) in the head and thorax altered their relative expression between the sexes as a result of mating. Sex-bias status changed in 2% of the genes in the abdomen and 4% in the head and thorax following mating. Mating responses involved de-feminization of females and, to a lesser extent, de-masculinization of males relative to their virgin state: mating decreased rather than increased dimorphic expression of sex-biased genes. The fact that regulatory changes of both types of sex-biased genes occurred in both sexes suggests that male-and female-specific selection is not restricted to male-and female-biased genes, respectively, as is sometimes assumed.

Keywords
RNA-Seq, transcriptome, sex-biased expression, sex-specific selection, alternative splicing
National Category
Genetics Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-326371 (URN)10.1093/gbe/evx029 (DOI)000402095700022 ()28391318 (PubMedID)
Funder
EU, European Research Council, AdG-294333Swedish Research Council, 621-2010-5266
Available from: 2017-07-07 Created: 2017-07-07 Last updated: 2018-08-10Bibliographically approved
Bayram, H. L., Sayadi, A., Goenaga, J., Immonen, E. & Arnqvist, G. (2017). Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach. Insect molecular biology (Print), 26(1), 58-73
Open this publication in new window or tab >>Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach
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2017 (English)In: Insect molecular biology (Print), ISSN 0962-1075, E-ISSN 1365-2583, Vol. 26, no 1, p. 58-73Article in journal (Refereed) Published
Abstract [en]

The seed beetle Callosobruchus maculatus is a significant agricultural pest and increasingly studied model of sexual conflict. Males possess genital spines that increase the transfer of seminal fluid proteins (SFPs) into the female body. As SFPs alter female behaviour and physiology, they are likely to modulate reproduction and sexual conflict in this species. Here, we identified SFPs using proteomics combined with a de novo transcriptome. A prior 2D-sodium dodecyl sulphate polyacrylamide gel electrophoresis analysis identified male accessory gland protein spots that were probably transferred to the female at mating. Proteomic analysis of these spots identified 98 proteins, a majority of which were also present within ejaculates collected from females. Standard annotation workflows revealed common functional groups for SFPs, including proteases and metabolic proteins. Transcriptomic analysis found 84 transcripts differentially expressed between the sexes. Notably, genes encoding 15 proteins were highly expressed in male abdomens and only negligibly expressed within females. Most of these sequences corresponded to 'unknown' proteins (nine of 15) and may represent rapidly evolving SFPs novel to seed beetles. Our combined analyses highlight 44 proteins for which there is strong evidence that they are SFPs. These results can inform further investigation, to better understand the molecular mechanisms of sexual conflict in seed beetles.

Keywords
evolution, reproduction, coleoptera, seminal fluid
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-315803 (URN)10.1111/imb.12271 (DOI)000391941200006 ()27779332 (PubMedID)
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266
Available from: 2017-02-22 Created: 2017-02-22 Last updated: 2018-08-10Bibliographically approved
Dordevic, M., Stojkovic, B., Savkovic, U., Immonen, E., Tucic, N., Lazarevic, J. & Arnqvist, G. (2017). Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles. Evolution, 71(2), 274-288
Open this publication in new window or tab >>Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles
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2017 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 2, p. 274-288Article in journal (Refereed) Published
Abstract [en]

The role of mitochondrial DNA for the evolution of life-history traits remains debated. We examined mitonuclear effects on the activity of the multisubunit complex of the electron transport chain (ETC) involved in oxidative phosphorylation (OXPHOS) across lines of the seed beetle Acanthoscelides obtectus selected for a short (E) or a long (L) life for more than >160 generations. We constructed and phenotyped mitonuclear introgression lines, which allowed us to assess the independent effects of the evolutionary history of the nuclear and the mitochondrial genome. The nuclear genome was responsible for the largest share of divergence seen in ageing. However, the mitochondrial genome also had sizeable effects, which were sex-specific and expressed primarily as epistatic interactions with the nuclear genome. The effects of mitonuclear disruption were largely consistent with mitonuclear coadaptation. Variation in ETC activity explained a large proportion of variance in ageing and life-history traits and this multivariate relationship differed somewhat between the sexes. In conclusion, mitonuclear epistasis has played an important role in the laboratory evolution of ETC complex activity, ageing, and life histories and these are closely associated. The mitonuclear architecture of evolved differences in life-history traits and mitochondrial bioenergetics was sex-specific.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
Bruchinae, coadaptation, epistasis, evolution of ageing, mitochondria, mtDNA, OXPHOS, senescence, sexual dimorphism
National Category
Ecology Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-320716 (URN)10.1111/evo.13109 (DOI)000394985200007 ()27861795 (PubMedID)
Funder
EU, European Research Council, AdG-294333Swedish Research Council, 621-2014-4523
Available from: 2017-04-24 Created: 2017-04-24 Last updated: 2018-08-10Bibliographically approved
Sayadi, A., Immonen, E., Tellgren-Roth, C. & Arnqvist, G. (2017). The Evolution of Dark Matter in the Mitogenome of Seed Beetles. Genome Biology and Evolution, 9(10), 2697-2706
Open this publication in new window or tab >>The Evolution of Dark Matter in the Mitogenome of Seed Beetles
2017 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 9, no 10, p. 2697-2706Article in journal (Refereed) Published
Abstract [en]

Animal mitogenomes are generally thought of as being economic and optimized for rapid replication and transcription. We use long-read sequencing technology to assemble the remarkable mitogenomes of four species of seed beetles. These are the largest circular mitogenomes ever assembled in insects, ranging from 24,496 to 26,613 bp in total length, and are exceptional in that some 40% consists of non-coding DNA. The size expansion is due to two very long intergenic spacers (LIGSs), rich in tandem repeats. The two LIGSs are present in all species but vary greatly in length (114-10,408 bp), show very low sequence similarity, divergent tandem repeat motifs, a very high AT content and concerted length evolution. The LIGSs have been retained for at least some 45 my but must have undergone repeated reductions and expansions, despite strong purifying selection on protein coding mtDNA genes. The LIGSs are located in two intergenic sites where a few recent studies of insects have also reported shorter LIGSs (>200 bp). These sites may represent spaces that tolerate neutral repeat array expansions or, alternatively, the LIGSs may function to allow a more economic translational machinery. Mitochondrial respiration in adult seed beetles is based almost exclusively on fatty acids, which reduces the need for building complex I of the oxidative phosphorylation pathway (NADH dehydrogenase). One possibility is thus that the LIGSs may allow depressed transcription of NAD genes. RNA sequencing showed that LIGSs are partly transcribed and transcriptional profiling suggested that all seven mtDNA NAD genes indeed show low levels of transcription and co-regulation of transcription across sexes and tissues.

Keywords
mitochondria, junk DNA, palindromes, Callosobruchus, Acanthoscelides, Bruchinae, intergenic spacers, metabolism, Coleoptera
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-341670 (URN)10.1093/gbe/evx205 (DOI)000414778600018 ()29048527 (PubMedID)
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2014-4523
Available from: 2018-02-13 Created: 2018-02-13 Last updated: 2018-08-10Bibliographically approved
Arnqvist, G., Stojkovic, B., Rönn, J. L. & Immonen, E. (2017). The pace-of-life: A sex-specific link between metabolic rate and life history in bean beetles. Functional Ecology, 31(12), 2299-2309
Open this publication in new window or tab >>The pace-of-life: A sex-specific link between metabolic rate and life history in bean beetles
2017 (English)In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 31, no 12, p. 2299-2309Article in journal (Refereed) Published
Abstract [en]
  1. Metabolic rate (MR) is a key functional trait simply because metabolism converts resources into population growth rate. Yet, our empirical understanding of the sources of within species variation in MR, as well as of its life history and ecological correlates, is rather limited. Here, we assess whether MR lies at the root of a syndrome of correlated rate-dependent life-history traits in an insect.
  2. Selection for early (E) or late (L) age-at-reproduction for >160 generations in the bean beetle Acanthoscelides obtectus has produced beetles that differ markedly in juvenile development, body size, fecundity schedules, ageing and life span. Here, we use micro-respirometry to test whether this has been associated with the evolution of age- and sex-specific metabolic phenotypes.
  3. We find that mass-specific MR is 18% higher in E lines compared to L lines and that MR decreases more rapidly with chronological, but not biological, age in E lines. Males, under sexual selection to “live-fast-die-young”, show 50% higher MR than females and MR decreased more rapidly with age in males.
  4. Our results are consistent with a central role for MR for the divergence in “pace-of-life” seen in these beetles, supporting the view that MR lies at the root of ecologically relevant life-history trait variation within species.
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-344046 (URN)10.1111/1365-2435.12927 (DOI)000416896700010 ()
Funder
Swedish Research Council, 621-2014-4523EU, European Research Council, GENCON AdG-294333
Available from: 2018-03-05 Created: 2018-03-05 Last updated: 2020-02-06Bibliographically approved
Immonen, E., Rönn, J., Watson, C., Berger, D. & Arnqvist, G. (2016). Complex mitonuclear interactions and metabolic costs of mating in male seed beetles. Journal of Evolutionary Biology, 29(2), 360-370
Open this publication in new window or tab >>Complex mitonuclear interactions and metabolic costs of mating in male seed beetles
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2016 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 29, no 2, p. 360-370Article in journal (Refereed) Published
Abstract [en]

The lack of evolutionary response to selection on mitochondrial genes through males predicts the evolution of nuclear genetic influence on male-specific mitochondrial function, for example by gene duplication and evolution of sex-specific expression of paralogs involved in metabolic pathways. Intergenomic epistasis may therefore be a prevalent feature of the genetic architecture of male-specific organismal function. Here, we assess the role of mitonuclear genetic variation for male metabolic phenotypes [metabolic rate and respiratory quotient (RQ)] associated with ejaculate renewal, in the seed beetle Callosobruchus maculatus, by assaying lines with crossed combinations of distinct mitochondrial haplotypes and nuclear lineages. We found a significant increase in metabolic rate following mating relative to virgin males. Moreover, processes associated with ejaculate renewal showed variation in metabolic rate that was affected by mitonuclear interactions. Mitochondrial haplotype influenced mating-related changes in RQ, but this pattern varied over time. Mitonuclear genotype and the energy spent during ejaculate production affected the weight of the ejaculate, but the strength of this effect varied across mitochondrial haplotypes showing that the genetic architecture of male-specific reproductive function is complex. Our findings unveil hitherto underappreciated metabolic costs of mating and ejaculate renewal, and provide the first empirical demonstration of mitonuclear epistasis on male reproductive metabolic processes.

Keywords
Callosobruchus maculatus, epistasis, metabolism, mitochondrial DNA, seed beetles, sex-specific selection
National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-280890 (URN)10.1111/jeb.12789 (DOI)000370070500012 ()26548644 (PubMedID)
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266
Available from: 2016-03-16 Created: 2016-03-16 Last updated: 2018-08-10Bibliographically approved
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Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0003-1121-6950

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