Measuring how sexual selection history impacts on population viability under genetic stress

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences

Abstract

Sexual selection occurs when individuals of one sex (usually males) compete for reproductive success. Darwin first recognised sexual selection as an force which could cause the evolution of elaborate traits that helped their bearers to gain individual reproductive success, either through male:male competition, female choice, or both. Since these early revelations, we have come to realise that sexual selection probably acts on most of an individual's traits and genes, because achieving reproductive success in the face of environmental stress requires a whole range of functional traits to be as adaptive as possible. Because of this, sexual selection might be relatively effective at filtering out individuals from a population who carry imperfect forms of genes or deleterious mutations.

We now know a great deal about how traits evolve through sexual selection, and what factors explain the dynamics of individual reproductive success, but we have placed far less effort into understanding the population consequences of sexual selection. This lack of attention needs to be changed, because it is population viability which underpins biodiversity and ecosystem stability, both of which are now suffering unprecedented and accelerating environmental stress as a result of human activities. This project will therefore measure the importance of sexual selection for creating populations that have superior viability in the face of stress.

Our general approach will be to use some unique lines of Tribolium flour beetles which we have carefully maintained under controlled conditions for 5 years at UEA, and where the only factor we have experimentally varied is the intensity and form of sexual selection. These lines will have therefore been subjected to experimental evolution across 65 generations, and they have already revealed some important insights into how individual males and females become adapted to different levels of sexual selection. We now propose to use these lines to measure how histories of high, medium, low and no sexual selection render populations resistant to extinction when they are placed under the genetic stress of inbreeding. Under inbreeding, when genetically related individuals are forced to reproduce, deleterious mutations are more likely to be exposed in offspring. This situation therefore provides a revealing measure of the underlying mutational load that a population is carrying. Inbreeding is now recognised to be a relevant force in the natural environment as populations become stressed and depleted, contributing to an 'extinction vortex' where populations can completely disappear.

Our hypothesis is that experimental populations which have been maintained under higher levels of sexual selection, where there are greater opportunities for male:male competition and female choice, should have been more effectively purged of deleterious genetic mutations, and so will maintain higher productivity and greater resistance to extinction under the stress of inbreeding. Our tests of productivity will be to measure the number of offspring generated per male-female pair in standard and poor environments, and our test of viability will be to measure extinction rates. As we increase the inbreeding level through sib-sib pairings down advancing generations, we will see our experimental populations becoming less viable as they reduce their productivity, and eventually go extinct. We predict that populations with a past history of heightened sexual selection should maintain productivity and resist extinction for longer than populations with no or low histories of sexual selection.

Our findings will not only provide valuable experimental insight into how sexual selection can filter deleterious mutations from the genome, but will also inform on the importance of sexual selection as a valuable force in the natural environment for maintaining the genetic health of small populations that are subjected to increasing stress.

Planned Impact

Who will benefit from this research?

There is a biodiversity crisis within the natural environment of planet earth where populations are experiencing accelerating stress and depletion as a result of human activities. Although there is an understandable focus on the phenotypes of populations, it is also essential that we appreciate and understand the underlying genetic architecture that allows populations to remain viable in the face of stress and depletion. This project investigates a widely-recognised natural process, sexual selection, and will measure whether it can play an influential role in improving the potential viability of populations when they are faced with stress and depletion. This process therefore has broad potential for far-reaching impact in the hugely-important area of understanding and managing the conservation of biodiversity. Because of this, not only does the project have impact for a wide range of environmental biologists, but it also applies to all of us who depend upon, and enjoy, the threatened biodiversity of planet earth. Ultimately, the research will address the question of whether the established natural process of sexual selection can improve the genetic 'health' of a population when it is placed under stress. The findings will have direct relevance to conservation managers working with small, endangered populations, and potentially identify another tool that could be used to manage or improve the genetic architecture of these small populations to allow them greater resistance to environmental stress.

How will they benefit from this research?

The fundamental route to generating impact is through publication of the primary research findings after peer-review in rapid turn-around, international-impact journals. Once this process is in train, we will use a wide range of possible communication outlets to ensure our findings reach a broad audience including: press releases, full popular media engagement (television, radio, print, web), WWW dissemination via high-impact visuals and video uploads linked to the journal website, and popular science outlets (including Planet Earth). We have experience of hitting all these targets when high-impact research is published, and the technician will receive media training and also engage.

In addition to printed publication of the primary findings, we will deliver talks at international conferences focusing on the overlapping fields of evolutionary biology and conservation biology, and budget for attendance at one of these on the requested resources. Depending on the exact findings, we will strive for impact among conservation practitioners and biodiversity NGO's, and if our results indicate major gains from a history of heightened sexual selection for small populations which then face stress, we will target our conference talk at a meeting which involves these conservation-focused end-users, such as the IUCN World Conservation Congress 2012 (Korea).

We will maintain an actively-updated and visually-exciting website for the project, with a live 'beetle-cam' which will allow visitors to see Tribolium adults interacting and competing for reproductive success. These visuals will be combined with explanations of how genetic architecture is important for biodiversity. More specifically, we will participate as active exhibitors in the Royal Society's Summer Science Exhibition in 2013, where results from this project will be combined with previous and ongoing related research using the Tribolium model in a display which explains and excites the public into appreciating the importance of using model organisms to understand broader processes in the natural environment.

Publications

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Godwin JL (2020) Mating patterns influence vulnerability to the extinction vortex. in Global change biology

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Hangartner S (2015) Experimental removal of sexual selection leads to decreased investment in an immune component in female Tribolium castaneum. in Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases

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Spurgin LG (2019) Conservation: The Costs of Inbreeding and of Being Inbred. in Current biology : CB

 
Description That sexual selection purges genetic load, and may partly explain why sexual reproduction is used by almost every animal species on Earth, despite its obvious costs.
That sexual selection improves male competitiveness and selects for the evolution of longer sperm.
That sexual selection improves population fitness as measured by its ability to genetically invade conspecific competitor populations.
Exploitation Route To conduct further analyses on genetic benefits of sexual selection for biodiversity and population fitness.
Sectors Environment

 
Description To understand the importance of evolved mating pattern to protect populations after genetic bottlenecks from inbreeding depression
First Year Of Impact 2011
Sector Environment
Impact Types Societal

 
Title Mating patterns influence vulnerability to the extinction vortex 
Description Earth's biodiversity is undergoing mass extinction due to anthropogenic compounding of environmental, demographic and genetic stresses. These different stresses can trap populations within a reinforcing feedback loop known as the extinction vortex, in which synergistic pressures build upon one another through time, driving down population viability. Sexual selection, the widespread evolutionary force arising from competition, choice and reproductive variance within animal mating patterns, could have vital consequences for population viability and the extinction vortex: 1) if sexual selection reinforces natural selection to fix 'good genes' and purge 'bad genes', then mating patterns encouraging competition and choice may help protect populations from extinction; 2) by contrast, if mating patterns create load through evolutionary or ecological conflict, then population viability could be further reduced by sexual selection. We test between these opposing theories using replicate populations of the model insect Tribolium castaneum exposed to over ten years of experimental evolution under monogamous versus polyandrous mating patterns. After a 95-generation history of divergence in sexual selection, we compared fitness and extinction of monogamous versus polyandrous populations through an experimental extinction vortex comprising 15 generations of cycling environmental and genetic stresses. Results showed that lineages from monogamous evolutionary backgrounds, with limited opportunities for sexual selection, showed rapid declines in fitness and complete extinction through the vortex. By contrast, fitness of populations from the history of polyandry, with stronger opportunities for sexual selection, declined slowly, with 60% of populations surviving by the study end. The three vortex stresses of i) nutritional deprivation, ii) thermal stress and iii) genetic bottlenecking had similar impacts on fitness declines and extinction risk, with an overall sigmoid decline in survival through time. We therefore reveal sexual selection as an important force behind lineages facing extinction threats, identifying the relevance of natural mating patterns for conservation management. 
Type Of Material Database/Collection of data 
Year Produced 2020 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.nzs7h44nz
 
Description Explanation of research findings 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Article reached broad scientific NERC audience

More planet earth articles requested
Year(s) Of Engagement Activity 2011,2014,2015
URL http://planetearth.nerc.ac.uk/news/story.aspx?id=1067
 
Description YouTube video 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Film inspired questions and contact

After broadcasting I was contacted online by a number of correspondents
Year(s) Of Engagement Activity 2011
URL https://www.uea.ac.uk/biological-sciences/people/profile/m-gage#researchTab