Animal population abundance and resilience: the role of polyandry and genome size as drivers of ecology.

Animal population abundance and resilience: the role of polyandry and genome size as drivers of ecology.

Hummingbird hawk-moth. Photo by Rob Knell

Understanding the factors that determine how species respond to threats such as climate change and habitat loss is crucial in predicting future trends and also in management of threatened species and habitats. Two potentially important factors in determining animal population abundance and resilience are the degree of (1) polyandry and (2) the size of the genome, but to date there have been virtually no tests of their effects. We propose to address these knowledge gaps using the British Lepidoptera (butterflies and moths) using several long-term monitoring schemes for these animals which have already been used to identify population trends for a large number of species1. This project will gather further data on British moths via a trapping programme plus a citizen science approach with amateur moth trappers contributing specimens, allowing the role of both these factors to be assessed with large, long-term datasets on each species.

  • In recent years it has become clear that strong precopulatory sexual selection, via female choice or intrasexual contests, can enhance adaptation rates and allow ‘evolutionary rescue’ when a population is faced with a changing environment2–4. There is, however, some evidence that postcopulatory sexual selection might have the opposite effect—ostracod species with larger sperm pumps are more likely to go extinct over geological time5 and dung beetle species with relatively large testes have reduced abundance in disturbed environments2. Whether this is a general effect is currently completely unknown. We will assess the degree of polyandry for a range of moth species by counting the spermatophores present in the reproductive tracts of freshly caught specimens — unlike other insect taxa the spermatophore membranes do not break down in the Lepidoptera6— and also by measuring relative testes size which is strongly correlated with the intensity of sperm competition7.
  • Genome size. Recent research has found that genome size is an important determinant of many aspects of plant ecology, such as growth rate and the response to nutrient levels8,9. These effects are thought to arise because genome size impacts minimal cell size, which in turn influences for example water loss, carbon dioxide assimilation, cell storage and cell wall strength10. In animals too, genome size influences their biology. There is evidence, for example, that genome size influences larval development and life history traits in frogs11 and it is correlated with reproductive success in seed beetles12. In addition, genome size is thought to be reduced in birds to facilitate flight13 and it impacts growth rate under limiting nutrients in freshwater snails14. Indeed, building and maintaining cells with large genomes may be more nutrient demanding than smaller ones, because nucleic acids are so rich in nitrogen and phosphorus. It is perhaps for this reason that genome size might impact food quality and feeding preferences15, perhaps because of the nutritional value of nucleic acids. Furthermore genome size may impact the production of anucleic sperm used in polyandrous moth species to pug the female reproductive tracks after mating and reduce the success of competing males. Potentially there might be selection for individuals to produce more anucleic sperm if they have a large genomes. Lepidopteran genome sizes vary nearly 10-fold (range from 0.215 Gb/1C to 1.897 Gb/1C) and we anticipate that across this range there will be effects on the biology of the insects. We will use existing data (e.g. from the Darwin Tree of Life project and the animal genome size database) and supplement this with measurements of genome sizes of other species. Host plant genome sizes are available on the Kew Plant DNA C-values database. Using these data we will will test the hypotheses that Lepidopteran genome size impacts growth rate, sexual system (polyandry), generation times and host range of the plants (see16 for a preliminary test of the last)

The long-term Lepidoteran data sets to be used will be the Rothamsted Insect Survey and the National Moth Recording Scheme. These datasets will give a combination of time-series data at specific locations (RIS) and occupancy data (NMRS, National Moth Recording Scheme) allowing us to develop statistical models to test the effects of polyandry and genome size on a suite of important aspects of the ecology of these animals. These results will provide a uniquely detailed assessment of these important questions with considerable potential for high-impact publications.


Caterpillar of the cinnabar moth feeding on ragwort. Photo by Rob Knell
  1. Fox R, Dennis EB, Harrower CA, Blumgart D, Bell JR, Cook P, Davis AM, Evans-Hill LJ, Haynes F, Hill D, Isaac NJB, Parsons MS, Pocock MJO, Prescott T, Randle Z, Shortall CR, Tordoff GM, Tuson D, Bourn NAD. The State of Britain’s Larger Moths 2021. (2021).
  2. Parrett, J. M., Mann, D. J., Chung, A. Y. C., Slade, E. M. & Knell, R. J. Sexual selection predicts the persistence of populations within altered environments. Ecol. Lett. 83, 238 (2019).
  3. Martínez-Ruiz, C. & Knell, R. J. Sexual selection can both increase and decrease extinction probability: reconciling demographic and evolutionary factors. J. Anim. Ecol. 86, 117–127 (2017).
  4. Cally, J. G., Stuart-Fox, D. & Holman, L. Meta-analytic evidence that sexual selection improves population fitness. Nat. Commun. 10, 2017 (2019).
  5. Martins, M. J. F., Puckett, T. M., Lockwood, R., Swaddle, J. P. & Hunt, G. High male sexual investment as a driver of extinction in fossil ostracods. Nature 556, 366–369 (2018).
  6. Gage, M. J. G. Associations between Body Size, Mating Pattern, Testis Size and Sperm Lengths across Butterflies. Proc. R. Soc. Lond. B Biol. Sci. 258, 247–254 (1994).
  7. Simmons, L. W. Sperm competition and its evolutionary consequences in the insects. (Princeton University Press, 2001).
  8. Guignard, M. S. et al. Genome size and ploidy influence angiosperm species’ biomass under nitrogen and phosphorus limitation. New Phytol. 210, 1195–1206 (2016).
  9. Faizullah, L. et al. Exploring environmental selection on genome size in angiosperms. Trends Plant Sci. 26, 1039–1049 (2021).
  10. Leitch, A. R. & Leitch, I. J. Genome evolution: On the nature of trade-offs with polyploidy and endopolyploidy. Current biology: CB vol. 32 R952–R954 (2022).
  11. Liedtke, H. C., Gower, D. J., Wilkinson, M. & Gomez-Mestre, I. Macroevolutionary shift in the size of amphibian genomes and the role of life history and climate. Nat Ecol Evol 2, 1792–1799 (2018).
  12. Arnqvist, G. et al. Genome size correlates with reproductive fitness in seed beetles. Proc. Biol. Sci. 282, (2015).
  13. Wright, N. A., Gregory, T. R. & Witt, C. C. Metabolic “engines” of flight drive genome size reduction in birds. Proc. Biol. Sci. 281, 20132780 (2014).
  14. Neiman, M., Kay, A. D. & Krist, A. C. Sensitivity to phosphorus limitation increases with ploidy level in a New Zealand snail. Evolution 67, 1511–1517 (2013).
  15. Solomon, J. K. Q., Macoon, B., Lang, D. J., Vann, R. C. & Ward, S. Cattle Grazing Preference among Tetraploid and Diploid Annual Ryegrass Cultivars. Crop Sci. 54, 430–438 (2014).
  16. Calatayud, P.-A. et al. Is genome size of Lepidoptera linked to host plant range? Entomol. Exp. Appl. 159, 354–361 (2016).