NSFDEB-NERC: Ecological Genomics of Adaptive Polymorphism

Lead Research Organisation: University of Sussex
Department Name: Sch of Life Sciences

Abstract

Accounting for high genetic diversity in ecologically-important traits is a fundamental problem in evolutionary biology. Individuals vary enormously at the genetic level, even within local populations, and we do not understand why. Recent work implicates an advantage to rare types as a critical factor maintaining genetic variation in many species, but we have little understanding of how this process actually unfolds in the wild. To address this gap, we need to (1) understand how ecological and social interactions promote or erode genetic diversity, and (2) link these interactions among organisms directly to the genes underlying the traits that mediate these interactions. This project will link a genetically diverse trait in the Trinidad guppy (Poecilia reticulata) to the ecological and social interactions that shape its evolution, and to the underlying genes that shape this diversity. Our previous work indicates that interactions with predators and with potential mates both favour rare colour patterns in this species. To determine which of the processes is most responsible for promoting diversity, we will collect data on predation risk and mating behaviour in multiple natural populations and relate these data to the degree of genetically-based diversity in colour patterns. Then, using populations and closely related species that vary in their genetic diversity, we will use whole-genome DNA sequencing to identify genes that control this highly variable trait. This will allow us to determine how ecological and molecular processes interact to promote or constrain evolution under balancing selection. Finally, we will directly test the idea that interactions between potential mates can maintain diversity in this species by observing evolution in real time in experimental populations with different opportunities for mate choice.

Planned Impact

The impact of this work will be primarily academic. Nevertheless, in addition to their academic interest, guppies are well suited for public outreach. They are highly charismatic because they are colourful, active, and engage in conspicuous courtship displays even in captivity. These fish are also well known to the general public because of their popularity in the pet trade. We have therefore developed an outreach program targeting schools in the UK and Trinidad. This outreach program involves a collaboration with the Asa Wright Nature Centre (AWNC) and through this collaboration we will enhance their capacity for outreach in the short-term. This will also be the basis for a long-term collaboration with AWNC to promote conservation and the world-class science being done in the northern mountain range of Trinidad. The collaboration also includes Amy Deacon at the University of the West Indies and her students/associates
We have developed a public outreach program that will engage students in science and introduce students to evolutionary theory with a focus on balancing selection. There are a number of reasons why this is important and beneficial for students. While many biology courses aim to present the massive amounts of biodiversity that exists, few answer the question why there is so much diversity. Natural selection, and balancing selection specifically, answers this question. Also, by introducing the students to our work we will challenge them to synthesize many different areas of biology beyond evolutionary biology; including genetics (understanding the rules of genetic inheritance), ecology (how species interact with each other) and animal behaviour (why do animals engage in different behaviours). Finally, this work, along with our public outreach package will dispel some common misconceptions about evolution: (i) that evolution is slow (in reality it can be so fast we can observe it directly, e.g. in our experiment proposed in Aim 3), (ii) that it only involves major phenotypic changes (small changes in appearance like colour pattern can have a large impact on the fitness of an individual and therefore the evolution of populations), and (iii) that evolution is a process towards one perfect 'well-designed' organism (in reality there are many possible optimal phenotypes, even in a single population, depending on the environment). To summarize, the goals of the presentation and activities will be to raise (i) the students' knowledge of evolution (especially directional and balancing selection) using guppies as an easily, accessible example, and (ii) their knowledge and appreciation of biodiversity and its intrinsic values, especially of tropical forests such as those in Trinidad. By teaching students about our work, we will have a lasting and significant impact on their understanding of evolution and nature and inspire them towards a life-long learning in science.
Capacity building
The PDRA based at the University of Sussex will be trained in a diverse set of transferable skills that will positioned them for future employment both within and outside of academia. The PDRA will also gain experience in disseminating research through oral presentations at international conferences as well as group meetings, and through manuscript preparation.
The PDRA and PI Fraser will also enhance their professional skillset by taking advantage of the training courses and events offered by the University of Sussex, including Sussex Impact Day, and media training (offered by the Science Media Centre). PI Fraser will also participate in the STEMnet training courses, such as, "Powerful Practicals" to learn how best to design a hands-on activity and "People Like Me", developed by the Women in Science and Engineering (WISE) campaign, to learn approaches designed specifically for girls ages 11-14 in mind.

Related Projects

Project Reference Relationship Related To Start End Award Value
NE/P013074/1 01/03/2017 29/09/2018 £415,117
NE/P013074/2 Transfer NE/P013074/1 30/09/2018 29/06/2021 £251,239
 
Description 1) Understanding the evolution of Y chromosomes is important for both evolutionary biology. Using a high quality genome assembly we were able to identify novel "Y" regions of the genome of guppies. This will further our understanding of how these fish evolve and how different sexes can display different traits despite having mostly the same genome. 2) We found that sex-linked colour variation is not only associated with the Y chromosome but with a large diverse haplotype on an autosome in guppies. Guppies are a classic system in sex chromosome evolution, and this substantially changes our understanding of how colour evolved.
Exploitation Route This will be of use to those studying balancing selection and sex chromosome evolution.
Sectors Other

 
Title On the genetic architecture of rapidly adapting and convergent life history traits in guppies 
Description The genetic basis of traits shapes and constrains how adaptation proceeds in nature; rapid adaptation can be facilitated by polygenic traits, which subsequently provide multiple, redundant, genetic routes to adaptive phenotypes, reducing re-use of the same genes (genetic convergence). Guppy life history traits evolve rapidly and convergently among natural high- (HP) and low-predation (LP) environments in northern Trinidad. This system has been studied extensively at the phenotypic level, but little is known about the underlying genetic architecture. Here, we use an F2 QTL design to examine the genetic basis of seven (five female, two male) guppy life history phenotypes to assess whether the genetic architecture of these traits reflects theoretical predictions. We use RAD-sequencing data (16,539 SNPs) from 370 male and 267 female F2 individuals. We perform linkage mapping, estimates of genome-wide and per-chromosome heritability (multi-locus associations), and QTL ma pping (single-locus associations). Our results are consistent with architectures of many-loci of small effect for male age and size at maturity and female interbrood period. Male trait associations are clustered on specific chromosomes, but female interbrood period exhibits a weak genome-wide signal suggesting a potentially highly polygenic component. Offspring weight and female size at maturity are also associated with a single significant QTL each. These results suggest rapid phenotypic evolution of guppies may be facilitated by polygenic trait architectures, but these could fuel redundancy and limit gene re-use across populations, in agreement with an absence of strong signatures of genetic convergence from recent population genomic analyses of wild HP-LP guppies. 
Type Of Material Database/Collection of data 
Year Produced 2022 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.w3r2280sk