IAP-24-102
Female mate choice, genetic effects, and the diverse reproductive strategies of live-bearing and egg-laying lizards
The evolution of mate choice has a major impact on dispersal strategies, fitness and, in the case of small populations, conservation and viability. When lizards select mates based on traits such as body size, colouration, or courtship behaviours, they drive sexual selection. This selection shapes the genetic landscape of a species and has impacts for the evolution of life history traits and behavioural strategies. Mate choice also impacts social dynamics and territory patterns, affecting how organisms interact with their habitat and influencing their ecological niche.
The Eurasian common lizard, Zootoca vivipara, is a fascinating model system for the evolution of reproductive choice and outcomes and their consequences for organismal biology. It is one of the only reproductively bimodal species, meaning that different lineages are either live-bearing or egg-laying. Amazingly, we have identified and characterised a case where these two parity modes are found in the same location and even hybridise (Recknagel et al. 2021). Not only the mode of reproduction differs between oviparous and viviparous lizards, but female investment also differs, such as the number and size of offspring (Recknagel and Elmer 2019). Thus oviparous, viviparous, and hybrid individuals are faced with different life history choices and trade-offs in reproduction.
Age can significantly influence mate choice in animals, including lizards, often shaping both preferences and mating success. The mate choice decisions lizards make, and the associated extent of polyandry of females, is predicted to change with age (Laloi et al. 2011). Females are often polyandrous and multiple paternity can elevate female fitness by providing more genetically diverse offspring, dilute the cost of mating with an incompatible or genetically inferior male, and bet-hedge against insufficient or poor-quality sperm. However, having multiple mating partners holds significant risks for females, such as in their interactions with males and exposure to disease during mating.
Life history theory suggests that the risks and strategies that a female takes in mating will vary depending her parity mode (i.e. being oviparous or viviparous) and on her age and health status. Further, her mate choice is affected by the males and the demography in her immediate area. The relative contributions of these factors have never been identified in a wild animal system contrasting parity modes. Additionally, the presence of hybrid females in the field allows tests of the incidence and reproductive fitness of females in a ZW sex-determination system, where we might expect Haldane’s Rule, one of the most extensively studied aspects of hybridisation, to be reversed and females show greater costs of hybridisation.
This project will study how oviparous and viviparous females differ in their reproductive strategies, how they trade-off costs and benefits, and the interaction of these individual-level decisions with parity mode evolution and population demography. To do so we will leverage this powerful comparison of lizards of two different parity modes that are living in the same environment, which mitigates confounds. This research will answer the following questions:
- How does reproductive investment and polyandry differ between oviparous and viviparous females and to what extent is it impacted by her age and health status?
- How does reproductive investment change across the female life span depending on her hybrid status?
- What is the population demography of oviparous and viviparous males and females on the landscape, and how is this projected to impact reproductive opportunities and outcomes?
Using these quantitative approaches to test theoretical expectations, the project will make a major contribution to our understanding of how benefits and costs across the life span interact with both genetic and behavioural life history trajectories.
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Image Captions
Field research on lizards and their reproductive biology
Methodology
The project, led and conducted by the student, will integrate organismal biology and molecular genomic analysis. In the field, lizards will be monitored over the breeding period to collect comprehensive data on females and their clutches. Reproductive decisions of females will be inferred from molecular approaches conducted in the lab, such as genetic analysis of offspring using genomic approaches with new and existing data (whole genome sequencing or ddRADseq). Parentage and pedigrees will be reconstructed based on genetic analysis of offspring, mothers, and the extant population.
Epigenomic analyses will be conducted based on DNA methylation (whole genome or targeted) of females to determine their age by developing and applying a novel ‘epigenetic clock’ for lizards. Demography of males in the population will be inferred from organismal data on size and fitness and molecular analysis of age (epigenomics) and genetic diversity (genomics). Reproductive output of parity modes will be examined in context of female age, size, and parity mode.
Project Timeline
Year 1
Literature review, transferrable skills training and development, molecular biology training and optimising protocols using existing bank of samples, initial development of epigenomic clock, fieldwork in Austria (3-4 months)
Year 2
Molecular biology approaches for parentage analysis and epigenomics, confirmation of epigenomic clock, fieldwork in Austria (3-4 months), transferrable skills training and development.
Year 3
Molecular analysis of parentage and epigenomics, analysis of demography and age data in context of life history; manuscript/thesis chapter writing; transferrable skills training and development; conference presentation.
Year 3.5
Data analysis; manuscript/thesis chapter writing; transferrable skills training and development; conference presentation
Training
& Skills
The student will receive well-rounded training in integrative biology, supported by the supervisory team (Elmer, Ritchie, Boonekamp) with expertise in evolutionary biology, reproductive biology, mate choice, ageing, and life history and will join an on-going and externally funded research project studying the ecology and evolution of reproduction. Training in fieldwork, lab work and analysis will be provided and additional opportunities supported. In the field, the student will learn sampling, husbandry, and morphological analyses for squamates. In the lab, the student will develop advanced molecular skills in genomic and epigenomic data generation. In analytical skills and interpretation, the student will develop advanced skills in genomic and epigenomic analysis. The student will be supported to develop critical thinking skills, conduct high quality research, disseminate results (through conferences, seminars, and manuscripts), and develop a well-rounded profile. The student will join an active and engaged research group with opportunities for discussion, support, and a collegial scientific environment.
References & further reading
Laloi, D., Eizaguirre, C., Fédérici, P., & Massot, M. (2011). Female choice for heterozygous mates changes along successive matings in a lizard. Behavioural Processes, 88(3), 149-154.
Moran, P. A., Ritchie, M. G. & Bailey, N. W. (2017). A rare exception to Haldane’s rule: Are X chromosomes key to hybrid incompatibilities? Heredity 118: 554-562.
Recknagel, H., & Elmer, K. R. (2019). Differential reproductive investment in co-occurring oviparous and viviparous common lizards (Zootoca vivipara) and implications for life-history trade-offs with viviparity. Oecologia, 190, 85-98.
Recknagel, H., Carruthers, M., Yurchenko, A. A., Nokhbatolfoghahai, M., Kamenos, N. A., Bain, M. M., & Elmer, K. R. (2021). The functional genetic architecture of egg-laying and live-bearing reproduction in common lizards. Nature Ecology and Evolution, 5(11), 1546-1556.
Richard, M., Losdat, S., Lecomte, J., de Fraipont, M., & Clobert, J. (2009). Optimal level of inbreeding in the common lizard. Proc Biol Sci, 276(1668), 2779-2786.
Rodríguez-Muñoz Rolando, Boonekamp Jelle J., Fisher David, Hopwood Paul and Tregenza Tom 2019 Slower senescence in a wild insect population in years with a more female-biased sex ratio. Proc. R. Soc. B.28620190286 http://doi.org/10.1098/rspb.2019.0286
Yusuf, L. H., Lemus, Y. S., Thorpe, P., Garcia, C. M. & Ritchie, M. G. 2023. Genomic signatures associated with transitions to viviparity in Cyprinodontiformes. Molecular Biology and Evolution 40: msad208.
