A proteomics approach to quantify adaptive variation in mammalian ejaculates

Lead Research Organisation: University of Liverpool
Department Name: Veterinary Preclinical Science

Abstract

This project addresses the role of seminal fluid proteins in mammalian sperm competition. Sperm competition occurs when the ejaculates of different males compete to fertilize a given set of ova. This is a pervasive selection pressure in the evolution of ejaculate characteristics and other reproductive traits for diverse animal taxa. In particular, it is now well established that male investment in the sperm component of ejaculates is strongly influenced by sperm competition. However, sperm usually make up only a tiny fraction of total ejaculate volume (1-5% for humans) compared to seminal fluid. Since proteins in the seminal fluid are essential to male fertilization success, it is likely that male investment in non-sperm components of the ejaculate will also be critical to determining sperm competition outcomes. Hence, to maximize fertilization success, males should tailor both the sperm and seminal fluid components of their ejaculates according to competitive conditions. To test this, we will combine advanced quantitative proteomics techniques with carefully controlled experiments using rodent models. Recently, we have demonstrated remarkable diversity in the seminal fluid proteins of muroid rodents, consistent with rapid evolution under sperm competition. To test for evidence of adaptive plasticity in ejaculate components, as predicted by sperm competition theory, we propose a systematic exploration of how investment in these proteins varies within species according to competitive risk. For the first time in any animal group, the application of advanced quantitative proteomics methodologies will allow us to precisely quantify variation in both seminal fluid protein and sperm content of the ejaculate when sperm competition is experimentally manipulated under controlled conditions. We will test for adaptive variation in the relative and total amount of seminal fluid proteins in rodent ejaculates, and quantify their relationships with sperm numbers. Specifically, we will determine ejaculate investment strategies according to (1) cues of sperm competition risk at the time of mating, (2) population-average sperm competition risk or intensity and (3) male dominance status. As well as testing for predicted changes in the ejaculate content of proteins with known functions, our research programme will reveal if other seminal fluid proteins vary consistently in relation to competitive conditions, and thus identify further candidate proteins with likely functional roles in sperm competition. These findings will establish the role of seminal fluid proteins in adaptive variation of mammalian ejaculate composition. To assess the fitness consequences of different ejaculate investment strategies, we will determine reproductive success for males mating under competitive conditions. This will provide insight into the functional significance of adaptive variation in mammalian ejaculate composition. These findings will have general relevance to understanding the functional and evolutionary consequences of adaptive variation in mammalian ejaculate composition.

Publications

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Bayram HL (2020) Social status and ejaculate composition in the house mouse. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

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Bayram HL (2016) Cross-species proteomics in analysis of mammalian sperm proteins. in Journal of proteomics

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Claydon A (2014) Quantitative Proteomics -

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Claydon AJ (2012) Proteome dynamics: revisiting turnover with a global perspective. in Molecular & cellular proteomics : MCP

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Edward DA (2014) Sexual conflict and sperm competition. in Cold Spring Harbor perspectives in biology

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Hammond DE (2016) Proteome Dynamics: Tissue Variation in the Kinetics of Proteostasis in Intact Animals. in Molecular & cellular proteomics : MCP

 
Description • Significant new knowledge generated
Results of our quantitative proteomics analyses provide clear evidence of adaptive plasticity in mammalian seminal fluid proteins under competitive conditions. Our findings also reveal significant fitness consequences of varying investment in seminal fluid production and ejaculate composition.

• New or improved research methods or skills developed
We have applied novel proteomics methods to provide qualitative profiling and precise quantitative measures of competing ejaculates within the female reproductive tract. The methods we have developed for use with rodent models can now be applied to determine adaptive variation in ejaculate composition across diverse taxa.

• Important new research questions opened up
We have identified mammalian seminal fluid proteins that are particularly responsive to the social environment - i.e. whose production is altered significantly in response to competitive conditions and male phenotype. In most cases the functions of these proteins are still not well understood, and our research suggests important roles in sperm competition as a priority for future investigation.

• Increased research capability linked to training
The project has provided unique interdisciplinary training for the PDRAs and associated PhD student. This training is now being applied in a government research agency setting (Food and Environment Research Agency) by our proteomics PDRA, and has facilitated an international research placement and prestigious PDRA position at a world-leading laboratory for our PhD student.

• Summary information
The original aims and objectives of the grant have been met. To date 14 published outputs are linked to the project. The team has engaged in multiple engagement activities, including KE with a major international animal breeding company and an associated international research placement. Interdisciplinary training provided during the project is now being applied both in a UK government research environment and internationally, via next destination positions of our team. The work has also received early recognition via international plenary and research talk invitations.
Exploitation Route The primary academic beneficiaries will be researchers in the fields of evolutionary biology, reproduction and fertility. For example, our findings can be applied to advance understanding of developmental and phenotypic plasticity, of benefit to predict how animals will respond to environmental change. Understanding of fundamental reproductive processes can also be advanced based on new insights into the role of seminal fluid proteins in enhancing male fertility.

Knowledge arising from this research can be applied to benefit the wealth, competitiveness and health of the nation via applications to the UK farming industry, and to human and veterinary medicine. Farming industries can benefit from application of knowledge to improve the efficiency of artificial insemination technologies and food animal productivity. Human and veterinary medicine can benefit from application of knowledge to diagnose and treat fertility problems and to improve techniques for assisted reproduction. Quality of life can also be enhanced by knowledge resulting from this research through benefits to animal conservation and increased public understanding of science.
Sectors Agriculture, Food and Drink,Education,Environment,Healthcare,Leisure Activities, including Sports, Recreation and Tourism,Pharmaceuticals and Medical Biotechnology,Other

URL https://bmcbiol.biomedcentral.com/articles/10.1186/s12915-015-0197-2
 
Description BBSRC CASE studentship
Amount £90,000 (GBP)
Organisation Genus plc 
Sector Private
Country United Kingdom
Start 10/2011 
End 12/2014
 
Description Collaboration Genus plc 
Organisation Genus plc
Country United Kingdom 
Sector Private 
PI Contribution Expertise in proteomics and reproductive biology.
Collaborator Contribution Expertise in commercial animal breeding, training opportunities for CASE PhD student.
Impact Multi-disciplinary collaboration (proteomics, genetics, evolutionary biology) leading to one published paper, with further publications in preparation.
Start Year 2010
 
Description 'Bioinspire' workshop (Knowsley) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Workshop stimulated discussion of ideas for biology themed visitor attraction and education centre based in Knowsley, Merseyside.

After the workshop, ideas were taken forward for further development.
Year(s) Of Engagement Activity 2014
URL http://www.newzoo.org.uk/?page_id=28
 
Description Media interest (BBC website) 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Input to journalist helped with producing BBC Science webpage.

Broad media interest in topic covered.
Year(s) Of Engagement Activity 2014
URL http://www.bbc.com/earth/bespoke/story/20140908-twisted-world-of-sexual-organs/index.html
 
Description Six-form school visit (Leahurst) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact Talk sparked questions and discussion afterwards.

Not known.
Year(s) Of Engagement Activity 2013
 
Description Veterinary training (Liverpool) 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Talk sparked questions and discussion afterwards

Organiser reported interest and subsequent discussion among participants
Year(s) Of Engagement Activity 2013