Final Report Summary - SEX SEL - VAR (Sexual selection - How is variation maintained?)
Understanding how genetic variation is maintained in natural populations is vital for our understanding of the process of evolution, since natural selection acts on the variation between individuals. Through sexual selection, females are thought to choose males with the most striking displays, which are heritable, leading to exaggerated male traits. However, if females always choose the ‘best’ males for heritable traits, this would drive a rapid and seemingly deleterious decrease in genetic diversity among males. This problem – known as the ‘lek paradox’ – is of fundamental importance because understanding this process will help us understand how genetic diversity is maintained.
Sexual selection is a key driving force behind the development and maintenance of exaggerated traits, adaptation to new environments, speciation, and animal breeding. This study combines lab, field, state-of-the-art genetic techniques and theoretical modeling in a truly integrative project, which will considerably further our understanding of sexual selection and the maintenance of variation.
Wild great tits (Parus major) were tested for their individual mate preference functions in the lab, by presenting them with unknown partners. Their preference function describes how much they are attracted to different aspects of a mates appearance or genetic quality. Many aspects of both the choosers and partners phenotype and genotype were measured, for example plumage characters, personality (exploratory behaviour), and genetic heterogysosity. This reveals for the first time that individuals differ in their preference, and this depends on the choosers own phenotype. We found assortative preference for heterozygosity and are currently investigating preferences for plumage traits. The choosing individuals were then followed while breeding the following Spring, to assess reproductive investment with the partner they actually pair with. This is the first time that individual differences in mate choice behaviour have been followed up in the wild. If individuals actually paired with a mate with the preferred level of heterozygosity, they were more successful at rearing offspring.
We are currently modeling how individual differences in mate preference contribute to genetic and phenotypic diversity. Additionally, we are preparing to submit a paper outlining how individuals choose, since in our study they appear to use a combination of absolute verses relative choice. Since starting this project, Camilla Hinde has built her research group at Wageningen University and attained tenure at Associate Professor level.
A key novel aspect of this project is the concept of detailing avian individual preference functions in the lab, and following the same individuals in the wild. We investigated preferences for heterozygosity in the lab, and the effects of this preference in the wild. This study was published in the journal Ecology Letters (impact factor 10.7). In brief, this article reports assortative mating preferences for heterozygosity in the lab. Time spent with a stimulus bird was influenced by an interaction between the chooser’s and stimulus birds’ heterozygosity (HLfocal * HLstimulus, GLMM: F1,62.93=2.76 P=0.008 see Fig. 2). Heterozygous birds spent more time with heterozygous birds, and vice versa, homozygous birds spent more time with homozygous birds. However this preference was not realized in mate choice (who individuals ended up pairing with) in the wild. Birds did not mate assortatively for heterozygosity. There was no difference between heterozygosity correlations within pairs and a randomly generated distribution of pairs drawn from the population (random correlation 95% confidence interval = [-0.23 0.25]; correlation breeding pairs = -0.07; N=70 breeding pairs; 10000 permutations). The difference between mate preference and pairing patterns in the wild could reflect the fact that in reality, availability of mates is very limited. Once paired, individuals are no longer available for pairing with another partner, so great tits may not always get their first choice.
Following the focal birds in the wild revealed that if they do get a partner similar to their preference, they enjoyed greater reproductive success. The relatedness of foster parents showed a quadratic relationship with fledging weight (on day 14); very unrelated and very related foster parents reared heavier offspring (relatedness2, LMM: t34.91=3.19 P=0.003). Cross fostering chicks between nests revealed that this effect was due to the provisioning behavior of the parents, rather than a genetic or pre hatching effect because chicks grew better if their foster parents had similar heterozygosity levels.
It was impossible to make accurate preference functions without investigating how parents choose – whether by responding to absolute trait values, or relative values between individuals (see attached manuscript: Measuring mate preferences: Absolute versus comparative evaluation of potential partners). We found that great tits use a combination of absolute and comparative evaluation and that the social context can affect the measured responses to stimulus groups of conspecifics. With such knowledge of how a study species encounters and evaluates potential mates, it is possible to choose the most appropriate experimental design and analysis to obtain reliable measurements of mate preferences. The ability to more accurately quantify preference is expected to increase our understanding of mate preferences, mate choice, and ultimately sexual selection.
In addition to a fully funded PhD student, supported by the University, my chair group has also
matched funds for a 1 year post doc. This is a spin-off project using the data from the current project
to investigate how sexual selection affects turn taking in parental care. Results for this project are
currently being written up as part of a special issue in “Frontiers in Ecology and Evolution”, which I am co-editing with collaborators Rufus Johnstone and James Savage.
Advancement beyond the state of the art in the field
This study combines lab, field, state-of-the-art genetic techniques and theoretical modeling in a truly integrative project, which will further our understanding of sexual selection and the maintenance of genetic variation in natural populations. The concept is novel and has brought together international researchers in a synergistic project.
Original concepts
This project introduces a novel concept, namely that variation can be maintained by individual differences in mate choice, and that mate preferences may vary in relation to the choosers own phenotype. Individual differences have previously been overlooked in the search for population-wide trends, and this study proposes a new, multidisciplinary approach to understanding the maintenance of variation. In building up this ‘big picture’, several other key concepts will be introduced. First, recent review articles have asked for a broader understanding of individual differences in mate choice see e.g. 1. This study takes up that challenge by testing the novel concept that individuals will vary their mate preference functions. Second, mate choice in the wild is usually measured by assuming individuals choose their preferred mate. This study does not make that assumption and introduces the idea that instead individuals may instead vary allocation in the young according to how close the partner they actually get is to their preference.
Impact
This project is contributing to European research excellence in three main ways. First, by producing high impact research. This research project addresses timely questions within one framework, which proposes a new, multidisciplinary approach to understanding the maintenance of variation. Due to the multidisciplinary nature of the work, the results are of broad interest scientifically, and has already led to high impact scientific papers (Zandberg et al. 2016, Caro et al. 2016)3,4.
Second, by inspiring and training student and intern scientists. Wageningen has a thriving student community, and the Masters and Undergraduate behavioural ecology courses have a strong research component. We have already had 30+ students and interns on the project, one of which has already secured a PhD position at Antwerp University. We will continue to involve Masters and BSc students, who can potentially continue their career within Wageningen, the Universities and research institutes involved in the collaboration, or other centers within the EU.
Third, this project is structured around a multidisciplinary integrative framework and brings together researchers from across the EU (see above). A strong collaborative foundation will strengthen links within the EU scientific community and maximize the scientific impact of the proposal. This framework will cement relations between both diverse locations and disciplines, and establish myself as a prominent group leader.
Project website: https://www.wur.nl/en/Expertise-Services/Chair-groups/Animal-Sciences/Behavioural-Ecology-Group/Research/Behavioural-Ecology-1/Sexual-Selection-Project.htm
Sexual selection is a key driving force behind the development and maintenance of exaggerated traits, adaptation to new environments, speciation, and animal breeding. This study combines lab, field, state-of-the-art genetic techniques and theoretical modeling in a truly integrative project, which will considerably further our understanding of sexual selection and the maintenance of variation.
Wild great tits (Parus major) were tested for their individual mate preference functions in the lab, by presenting them with unknown partners. Their preference function describes how much they are attracted to different aspects of a mates appearance or genetic quality. Many aspects of both the choosers and partners phenotype and genotype were measured, for example plumage characters, personality (exploratory behaviour), and genetic heterogysosity. This reveals for the first time that individuals differ in their preference, and this depends on the choosers own phenotype. We found assortative preference for heterozygosity and are currently investigating preferences for plumage traits. The choosing individuals were then followed while breeding the following Spring, to assess reproductive investment with the partner they actually pair with. This is the first time that individual differences in mate choice behaviour have been followed up in the wild. If individuals actually paired with a mate with the preferred level of heterozygosity, they were more successful at rearing offspring.
We are currently modeling how individual differences in mate preference contribute to genetic and phenotypic diversity. Additionally, we are preparing to submit a paper outlining how individuals choose, since in our study they appear to use a combination of absolute verses relative choice. Since starting this project, Camilla Hinde has built her research group at Wageningen University and attained tenure at Associate Professor level.
A key novel aspect of this project is the concept of detailing avian individual preference functions in the lab, and following the same individuals in the wild. We investigated preferences for heterozygosity in the lab, and the effects of this preference in the wild. This study was published in the journal Ecology Letters (impact factor 10.7). In brief, this article reports assortative mating preferences for heterozygosity in the lab. Time spent with a stimulus bird was influenced by an interaction between the chooser’s and stimulus birds’ heterozygosity (HLfocal * HLstimulus, GLMM: F1,62.93=2.76 P=0.008 see Fig. 2). Heterozygous birds spent more time with heterozygous birds, and vice versa, homozygous birds spent more time with homozygous birds. However this preference was not realized in mate choice (who individuals ended up pairing with) in the wild. Birds did not mate assortatively for heterozygosity. There was no difference between heterozygosity correlations within pairs and a randomly generated distribution of pairs drawn from the population (random correlation 95% confidence interval = [-0.23 0.25]; correlation breeding pairs = -0.07; N=70 breeding pairs; 10000 permutations). The difference between mate preference and pairing patterns in the wild could reflect the fact that in reality, availability of mates is very limited. Once paired, individuals are no longer available for pairing with another partner, so great tits may not always get their first choice.
Following the focal birds in the wild revealed that if they do get a partner similar to their preference, they enjoyed greater reproductive success. The relatedness of foster parents showed a quadratic relationship with fledging weight (on day 14); very unrelated and very related foster parents reared heavier offspring (relatedness2, LMM: t34.91=3.19 P=0.003). Cross fostering chicks between nests revealed that this effect was due to the provisioning behavior of the parents, rather than a genetic or pre hatching effect because chicks grew better if their foster parents had similar heterozygosity levels.
It was impossible to make accurate preference functions without investigating how parents choose – whether by responding to absolute trait values, or relative values between individuals (see attached manuscript: Measuring mate preferences: Absolute versus comparative evaluation of potential partners). We found that great tits use a combination of absolute and comparative evaluation and that the social context can affect the measured responses to stimulus groups of conspecifics. With such knowledge of how a study species encounters and evaluates potential mates, it is possible to choose the most appropriate experimental design and analysis to obtain reliable measurements of mate preferences. The ability to more accurately quantify preference is expected to increase our understanding of mate preferences, mate choice, and ultimately sexual selection.
In addition to a fully funded PhD student, supported by the University, my chair group has also
matched funds for a 1 year post doc. This is a spin-off project using the data from the current project
to investigate how sexual selection affects turn taking in parental care. Results for this project are
currently being written up as part of a special issue in “Frontiers in Ecology and Evolution”, which I am co-editing with collaborators Rufus Johnstone and James Savage.
Advancement beyond the state of the art in the field
This study combines lab, field, state-of-the-art genetic techniques and theoretical modeling in a truly integrative project, which will further our understanding of sexual selection and the maintenance of genetic variation in natural populations. The concept is novel and has brought together international researchers in a synergistic project.
Original concepts
This project introduces a novel concept, namely that variation can be maintained by individual differences in mate choice, and that mate preferences may vary in relation to the choosers own phenotype. Individual differences have previously been overlooked in the search for population-wide trends, and this study proposes a new, multidisciplinary approach to understanding the maintenance of variation. In building up this ‘big picture’, several other key concepts will be introduced. First, recent review articles have asked for a broader understanding of individual differences in mate choice see e.g. 1. This study takes up that challenge by testing the novel concept that individuals will vary their mate preference functions. Second, mate choice in the wild is usually measured by assuming individuals choose their preferred mate. This study does not make that assumption and introduces the idea that instead individuals may instead vary allocation in the young according to how close the partner they actually get is to their preference.
Impact
This project is contributing to European research excellence in three main ways. First, by producing high impact research. This research project addresses timely questions within one framework, which proposes a new, multidisciplinary approach to understanding the maintenance of variation. Due to the multidisciplinary nature of the work, the results are of broad interest scientifically, and has already led to high impact scientific papers (Zandberg et al. 2016, Caro et al. 2016)3,4.
Second, by inspiring and training student and intern scientists. Wageningen has a thriving student community, and the Masters and Undergraduate behavioural ecology courses have a strong research component. We have already had 30+ students and interns on the project, one of which has already secured a PhD position at Antwerp University. We will continue to involve Masters and BSc students, who can potentially continue their career within Wageningen, the Universities and research institutes involved in the collaboration, or other centers within the EU.
Third, this project is structured around a multidisciplinary integrative framework and brings together researchers from across the EU (see above). A strong collaborative foundation will strengthen links within the EU scientific community and maximize the scientific impact of the proposal. This framework will cement relations between both diverse locations and disciplines, and establish myself as a prominent group leader.
Project website: https://www.wur.nl/en/Expertise-Services/Chair-groups/Animal-Sciences/Behavioural-Ecology-Group/Research/Behavioural-Ecology-1/Sexual-Selection-Project.htm