Sexual selection and the MHC in the fowl
Lead Research Organisation:
University of Oxford
Department Name: Zoology
Abstract
In many species females prefer to mate with specific males. In addition, when they mate with multiple males, females often favour fertilisation by the sperm of specific partners. Why do females favour certain males over others? It has been suggested that females may select males that carry genes which help the individual cope with their environment and by doing so the females thereby obtain the same high quality paternal genes for her young. This idea remains contentious and little tested. The major histocompatibility complex (MHC) is a group of genes that help determine resistance to parasites and diseases in higher animals (i.e. vertebrates, including humans). The type and variety of MHC genes an individual carries determine how well they can cope with parasites and diseases. Females may therefore increase the health of their offspring by selecting mates on the basis of MHC characteristics. This may happen in three different ways. First, females may favour fertilisations by males carrying an MHC that is different from their own. This will ensure that the offspring will inherit many different types of MHC genes (alleles) from their parents, and thus will be able to defend themselves from a wider range of diseases. Second, females may increase the MHC diversity of the offspring by favouring males that have a diverse MHC. Third, females may prefer males carrying specific MHC genes that provide more efficient resistance against diseases than other MHC types currently available. Understanding how MHC diversity influences reproduction is important for our understanding of the evolution of female mate choice, male sexual ornaments (e.g. stags antlers) and reproductive strategies. It may also allow us to better manage fertilisation and fertility problems in domestic and pest species and in species at risk of extinction. Despite much interest in the MHC and reproductive behaviour, the mechanisms through which the MHC may influence reproductive success remain unresolved. Our proposed research investigates the role of the MHC in the reproductive strategies of birds, and aims to determine if and how the different possible MHC-based mechanisms outlined above operate at specific reproductive stages: from mate choice to the selection of sperm within the female reproductive tract after insemination. We will study two semi-natural populations of fowl, Gallus gallus. The fowl is an ideal animal to study for two important reasons. First, it is a model system of reproductive physiology and behaviour and much is known about the mechanisms that determine mating and fertilisation success. Second, the MHC of the fowl is relatively small and easy to study. This has enabled extensive studies of the fowl MHC and its associations with disease resistance: more is known about the link between the MHC and diseases in the fowl than in any other animal. We will first: (a) determine how the MHC of males and/or their similarity with the females MHC females accounts for differences between the reproductive success of different males in small natural groups, (b) experimentally investigate how much the MHC determines male traits (e.g. social status, comb size and sperm quality) which influence a males ability to mate with females, and the fertilising efficiency of their ejaculates, (c) experimentally test whether female preference for certain mates is explained by MHC mechanisms. We will then focus on events occurring during/after insemination, by testing whether: (e) males invest more sperm in certain females based on female MHC characteristics, (f) females preferentially utilise the sperm of certain partners based on male MHC characteristics, and (g) the outcome of the competition between ejaculates that occurs when females copulate with multiple males (as it normally happens in the fowl), is determined by the MHC characteristics of males involved.
Organisations
Publications
Jensen P
(2008)
Genetics and genomics of animal behaviour and welfare-Challenges and possibilities
in Applied Animal Behaviour Science
Pizzari T
(2016)
The Wood-Gush legacy: A sociobiology perspective to fertility and welfare in chickens
in Applied Animal Behaviour Science
Parker GA
(2010)
Sperm competition and ejaculate economics.
in Biological reviews of the Cambridge Philosophical Society
Pizzari T
(2008)
Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time.
in BMC evolutionary biology
Foster KR
(2010)
Cooperation: the secret society of sperm.
in Current biology : CB
Pizzari T
(2009)
Sexual selection: sperm in the fast lane.
in Current biology : CB
Dean R
(2010)
Male reproductive senescence causes potential for sexual conflict over mating.
in Current biology : CB
Pizzari T
(2006)
Evolution: the paradox of sperm leviathans.
in Current biology : CB
Noguera J
(2012)
Age-specific oxidative status and the expression of pre- and postcopulatory sexually selected traits in male red junglefowl, G allus gallus
in Ecology and Evolution
McDonald G. C.
(2019)
Sexual selection in complex communities: integrating interspecific reproductive interference in structured populations
in Evolution
McDonald GC
(2019)
Sexual selection in complex communities: Integrating interspecific reproductive interference in structured populations.
in Evolution; international journal of organic evolution
Tan CK
(2013)
Parental age, gametic age, and inbreeding interact to modulate offspring viability in Drosophila melanogaster.
in Evolution; international journal of organic evolution
Worley K
(2008)
Single locus typing of MHC class I and class II B loci in a population of red jungle fowl.
in Immunogenetics
Worley K
(2010)
MHC heterozygosity and survival in red junglefowl.
in Molecular ecology
Carazo P
(2014)
Within-group male relatedness reduces harm to females in Drosophila.
in Nature
McDonald GC
(2013)
Sexual networks: measuring sexual selection in structured, polyandrous populations.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Carleial R
(2020)
Temporal dynamics of competitive fertilization in social groups of red junglefowl (Gallus gallus) shed new light on avian sperm competition.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Alonzo SH
(2013)
Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Pizzari T
(2013)
The polyandry revolution.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Pizzari T
(2012)
The sociobiology of sex: inclusive fitness consequences of inter-sexual interactions.
in Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Pizzari T
(2008)
Sperm sociality: cooperation, altruism, and spite.
in PLoS biology
Dean R
(2012)
Experimental evolution of a novel sexually antagonistic allele.
in PLoS genetics
Pizzari T
(2006)
Of mice and sperm.
in Proceedings of the National Academy of Sciences of the United States of America
Collet J
(2012)
Sexual selection and the differential effect of polyandry.
in Proceedings of the National Academy of Sciences of the United States of America
Løvlie H
(2013)
Cryptic female choice favours sperm from major histocompatibility complex-dissimilar males
in Proceedings of the Royal Society B: Biological Sciences
Gillingham MA
(2009)
Cryptic preference for MHC-dissimilar females in male red junglefowl, Gallus gallus.
in Proceedings. Biological sciences
Pizzari T
(2007)
Social competitiveness associated with rapid fluctuations in sperm quality in male fowl.
in Proceedings. Biological sciences
Collet JM
(2014)
The measure and significance of Bateman's principles.
in Proceedings. Biological sciences
Tan CK
(2013)
Sex-specific responses to sexual familiarity, and the role of olfaction in Drosophila.
in Proceedings. Biological sciences
Dean R
(2007)
Evolution. Aging and sexual conflict.
in Science (New York, N.Y.)
Pizzari T
(2007)
Post-insemination sexual selection in birds.
in Society of Reproduction and Fertility supplement
Alonzo SH
(2010)
Male fecundity stimulation: conflict and cooperation within and between the sexes: model analyses and coevolutionary dynamics.
in The American naturalist
Cornwallis CK
(2014)
Sex-specific patterns of aging in sexual ornaments and gametes.
in The American naturalist
Tazzyman SJ
(2009)
The evolution of continuous variation in ejaculate expenditure strategy.
in The American naturalist
Løvlie H
(2007)
Sex in the morning or in the evening? Females adjust daily mating patterns to the intensity of sexual harassment.
in The American naturalist
Dean R
(2011)
The risk and intensity of sperm ejection in female birds.
in The American naturalist
Pizzari T
(2008)
The evolutionary ecology of pre- and post-meiotic sperm senescence.
in Trends in ecology & evolution
Firman RC
(2017)
Cryptic Female Choice: A General Phenomenon. A Reply to Eberhard.
in Trends in ecology & evolution
Pizzari T, Bonduriansky R
(2009)
Social Behaviour: Genes, Ecology and Evolution
Pizzari T
(2009)
Sperm Biology
Birkhead TR & Pizzari T
(2007)
Biology of Breeding Poultry
Pizzari, T.
(2010)
Social Behaviour: Genes, Ecology and Evolution
Pizzari, T.
(2008)
Sperm Biology: An Evolutionary Perspective
Description | This was a split award between T Pizzari at Oxford (grant NE/D003865/1) and DS Richardson at UEA (grant NE/D002788/1), with Pizzari as the PI. The same key findings of this award have been entered for both, Oxford and UEA grants. Following advise from ROS Carl Kenneally, in the current report are included the most significant outcomes. A comprehensive list of the outcomes of this award (32 entries) has been submitted for NE/D002788/1. Aim 1. We conducted extensive monitoring of paternity skew in 12 replicate groups in which all birds were MHC-typed and characterised for multiple sexually-selected traits, as well as genetic relatedness. Preliminary results indicate a number of key novel features of sexually promiscuous mating systems, including the fact that female promiscuity reduces the overall opportunity for sexual selection while increasing the relative importance of post-insemination selective episodes. We also demonstrated an over-riding effect of male status in determining variation in reproductive success arising before and after insemination. However, after controlling for male status, we showed that pairs with lower genome-wide similarity had a reproductive advantage over pairs that were more genetically similar, indicating a role of MHC similarity as predictor of genome-wide similarity between prospective partners. Aim 2. We detected a strong signature of MHC heterozygosity in the ability of males and females to survive to reproductive maturity (Worley et al. 2010 Mol Ecol). Aim 3. We demonstrated experimentally that the genetic similarity effects outlined in Aim 1 are explained by both male and female preference for genetically dissimilar mating partners. Aim 4. We showed that male fowl allocate sperm differentially according to their MHC similarity with a female (Gillingham et al. 2009 Proc. R. Soc. B). Aim 5. We found that following the first inseminations, females tend to bias paternity in favour of MHC-similar ejaculates, and that over successive inseminations this bias is reversed towards MHC-dissimilar males. Aim 6. We found strong 'transitive' seminal fluid effects, whereby the seminal fluid of an ejaculate with high sperm velocity increases the sperm velocity of another ejaculate with initially lower sperm velocity, and vice versa. Importantly, we also found that these effects were significantly more marked when seminal fluid and sperm donor males had intermediate MHC similarity. |
Exploitation Route | These findings represent a platform to refine the role of MHC in: differential female responses (e.g. immune-mediated) to sperm, social recognition (e.g. kin and familiarity cues) and pathogen resistance. Our research group is actively pursuing these lines of research. Specifically these findings have informed collaboration with Prof Jim Kaufman (Cambridge) to type the MHC of the red junglefowl population and study patterns of MHC II expression (ms under review in Frontiers in Immunology). This collaboration has contributed to a recent EU2020 grant application coordinated by the PI (unsuccessful). |
Sectors | Agriculture, Food and Drink,Education |
Description | These results have critical importance for the management of fertility in commercial flocks and have led to a close partnership between the PI and AVIAGEN, a leading industry in the global poultry market. This partnership has already resulted in a CASE NERC/EPSRC PhD project to explore the mechanisms underpinning variation in fertility in AVIAGEN broiler breeder flocks, and we are now in the process to apply for a 'Stand Alone' LINK BBSRC grant to resolve these issues. These results provide a unique insight into the complex dynamics that govern variation in fertilisation success within populations and indicate a potentially important role for MHC similarity and immunity. These findings have led to a follow-on research NERC grant (NE/H008047/1) to explore more explicitly the link between MHC and female immune responses to antigenic properties of sperm in fertilisation dynamics (in collaboration with molecular ecologist David Richardson at UEA and immunologist Adrian Smith at Oxford). This work has also led to new collaborations with Prof Jim Kaufman (Cambridge), Dr Lorna Kennedy (Manchester). |
First Year Of Impact | 2006 |
Impact Types | Societal |
Description | NSERC Postdoctoral Fellowship |
Amount | $80,000 (CAD) |
Organisation | Natural Sciences and Engineering Research Council of Canada (NSERC) |
Sector | Public |
Country | Canada |
Start | 01/2011 |
End | 09/2013 |
Description | PhD Scholarship to study fertility in fowl populations |
Amount | £100,000 (GBP) |
Organisation | Oxford Environmental Research DTP |
Sector | Academic/University |
Country | United Kingdom |
Start | 10/2019 |
End | 09/2023 |
Description | Royal Society International Incoming Short Visits |
Amount | £4,500 (GBP) |
Organisation | The Royal Society |
Sector | Charity/Non Profit |
Country | United Kingdom |
Start |
Description | Media communication |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | Yes |
Geographic Reach | National |
Primary Audience | Public/other audiences |
Results and Impact | My understanding is that the BBC series was well received and sparked interest in the behaviour and welfare of domestic animals Difficult to quantify impact of this contribution to the series as a whole. |
Year(s) Of Engagement Activity | 2009 |
Description | Media communication |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Media (as a channel to the public) |
Results and Impact | Interview on MHC-mediated cryptic female choice for Jack FM Radio No notable impact |
Year(s) Of Engagement Activity | 2013 |
Description | Media communication BBC Radio 4 |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | No |
Geographic Reach | National |
Primary Audience | Media (as a channel to the public) |
Results and Impact | Interview for the programme "The hunt of the Gay whale" After my interview I was contacted by peers and members of the public to discuss the subject further. |
Year(s) Of Engagement Activity | 2012 |
URL | http://www.bbc.co.uk/programmes/b01k1mwp |
Description | Talk at local primary school (S.S. Mary and John, Oxford) |
Form Of Engagement Activity | A talk or presentation |
Part Of Official Scheme? | No |
Geographic Reach | Local |
Primary Audience | Schools |
Results and Impact | ~50 pupils and several teaching staff attended this |
Year(s) Of Engagement Activity | 2016 |
Description | media communication |
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 | Media (as a channel to the public) |
Results and Impact | Interview on our work on MHC-mediated cryptic female choice for University of Oxford Press Office. This led other media contacting me for interviews. |
Year(s) Of Engagement Activity | 2013 |
URL | http://www.ox.ac.uk/news/2013-01-21-sexual-networks-reveal-complex-mating-game |
Description | media communication |
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 | Media (as a channel to the public) |
Results and Impact | Interview on our work on sexual selection for ABC Radio Australia Science Show no notable impact |
Year(s) Of Engagement Activity | 2013 |
URL | http://www.abc.net.au/radionational/programs/scienceshow/polyandry-brings-evolutionary-rewards-in-th... |
Description | media communication |
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 | Media (as a channel to the public) |
Results and Impact | Interview on sexual selection for NRC Handelsblad Science Desk Interview. Difficult to quantify the impact of this activity. |
Year(s) Of Engagement Activity | 2013 |
Description | media communication |
Form Of Engagement Activity | A press release, press conference or response to a media enquiry/interview |
Part Of Official Scheme? | No |
Geographic Reach | Regional |
Primary Audience | Media (as a channel to the public) |
Results and Impact | Radio Interview for BBC Oxford on recent findings of my research After my interview, I was contacted by colleagues and members of the general public to discuss the topic further. |
Year(s) Of Engagement Activity | 2013 |