How have animal genitalia co-diversified between the sexes? Linking biomechanics to genital evolution in insects
Final Report Abstract
The rapid divergence of genitalia is a prevailing trend among internal inseminators. The evolutionary processes have received burgeoning attention over the past few decades. Considerable empirical and theoretical research suggests that sexual selection is a major driving force of genital diversification. However, previously largely neglected hypotheses, i.e., lock and key, natural selection and pleiotropy have recently been revisited. The question of which driving forces play a significant role in genital diversification remains actively discussed. Despite the plethora of previous research on genital diversification, the linkage between diverse genital structures and their functionality has rarely been studied. Importantly, selection forces do not act directly on morphological characteristics but rather via functionality. Therefore, my collaboration partners and I have been examining the biomechanics of male and female genital interactions in insects. Despite technical challenges due to the smallness of the focusing structures, we successfully overcame challenges in many cases and established the basis of the biomechanics of genitals in arthropods. In the two-phased project granted by the DFG, the following three steps of male and female reproductive interactions were deeply investigated: penetration, ejaculation, and sperm storage. We tried to find the mechanical causations of male and female sexual interactions by means of combinations of modern microscopy techniques, material distribution analyses, and theoretical calculations. Our project is not finished yet due to the move of my working place from Germany to Japan; nevertheless, our biomechanical studies on male and female sexual interactions showed the followings which cannot be even expected only by observing the morphology: (1) The elongated male and female genitalia are the simplest system of the whole genitalia. Therefore, the sexual interaction of elongated male and female genitalia appears very simple, the penetration mechanics is, however, achieved by the combination of specific structural and physical properties of the genitalia, e.g. material heterogeneity and flexibility of male and female elongated genitalia. We studied the penetration mechanics of the elongated male and female genitalia of two distantly related insect groups including species with hyper-elongated genitalia and with very shortly elongated genitalia. Species with hyper-elongated genitalia showed a similar set of specialisations irrespective of the phylogenetic background, while species with very shortly elongated genitalia were not the case. (2) Our studies on ejaculation and sperm storage processes suggested that quantitative shape variations could largely change its functionality. These findings brought us a constraint hypothesis that states among quantitative variations seen in closely related species, there are hypothetical male and female genital combinations with lower functionality, which could be an intrinsic mechanism for the co-diversification of genitalia under the abovementioned variable driving forces. The ultimate goal of our ongoing project is now to test this hypothesis. To accomplish this goal, we will increase examples of biomechanical studies on the genitalia and link not only realistic quantitative variations of genitalia but also hypothetical (absent in nature) ones with potential functionalities by conducting mechanical tests with artificial models, e.g., 3D-printed male and female genitalia with variable shapes and materials will be used to simulate the penetration process with different structural and material properties. Consequently, we will be able to compare the functionalities between realistic and hypothetical genitalia to test the hypothesis.
Publications
- (2017) Functional morphology and evolution of the hyper-elongated intromittent organ in Cassida leaf beetles (Coleoptera: Chrysomelidae: Cassidinae). Zoology 120, 1–14
Matsumura Y., Michels J., Appel E., Gorb S.N.
(See online at https://doi.org/10.1016/j.zool.2016.08.001) - (2017) Penetration mechanics of a beetle intromittent organ with bending stiffness gradient and a soft tip. Science Advances 3, eaao5469
Matsumura Y., Kovalev A., Gorb S.N.
(See online at https://doi.org/10.1126/sciadv.aao5469) - (2017) Surface-contacts during mating in beetles: stiffness gradient of the beetle penis facilitates propulsion in the spiraled female spermathecal duct. In: Functional Surfaces in Biology III (pp. 247-262). Springer, Cham
Matsumura Y., Kovalev A.E., Filippov A.E., Gorb S.N.
(See online at https://doi.org/10.1007/978-3-319-74144-4_11) - (2017) Traumatic mating by hand saw-like spines on the internal sac in Pyrrhalta maculicollis (Coleoptera, Chrysomelidae, Galerucinae). Zookeys 720, 77–89
Matsumura Y., Suenaga H., Kamimura Y., Gorb S.N.
(See online at https://doi.org/10.3897/zookeys.720.13015) - (2019) Sperm transfer through hyper-elongated beetle penises – morphology and theoretical approaches. Scientific Reports 9, 10238
Matsumura Y., Michels J., Rajabi H., Shimozawa T., Gorb S.N.
(See online at https://doi.org/10.1038/s41598-019-46211-x) - (2020) 3D printed spermathecae as experimental models to understand sperm dynamics in leaf beetles. BMC Zoology 5, 9
Matsumura Y., Gürke S., Tramsen H.T., Gorb S.N.
(See online at https://doi.org/10.1186/s40850-020-00058-2) - (2020) Material heterogeneity of male genitalia reduces genital damage in a bushcricket during sperm removal behaviour. The Science of Nature, 107, 52
Matsumura Y., Jafarpour M., Ramm S.A., Reinhold K., Gorb S.N., Rajabi H.
(See online at https://doi.org/10.1007/s00114-020-01706-w) - (2021) Excavation mechanics of the elongated female rostrum of the acorn weevil Curculio glandium (Coleoptera; Curculionidae). Applied Physics A, 127(5), 1-11
Matsumura Y., Jafarpour M., Reut M., Shams Moattar B., Darvizeh A., Gorb S.N., Rajabi H.
(See online at https://doi.org/10.1007/s00339-021-04353-8) - (2021) Penetration mechanics of elongated female and male genitalia of earwigs. Scientific Reports, 11(1), 1-17
Matsumura Y., Kamimura Y., Lee C.-Y., Gorb S.N., Rajabi H.
(See online at https://doi.org/10.1038/s41598-021-86864-1) - (2021). Mechanical properties of a female reproductive tract of a beetle and implications for penile penetration. Proceedings of the Royal Society B, 288(1954), 20211125
Matsumura Y., Kovalev A., & Gorb S.N.
(See online at https://doi.org/10.1098/rspb.2021.1125)
