How have animal genitalia co-diversified between the sexes? Linking biomechanics to genital evolution in insects

• Applicant: Dr. Yoko Matsumura
• Subject Area: Systematics and Morphology (Zoology)
• Term: from 2017 to 2022
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 373428351

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, 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 and found that their quantitative shape variations can largely alter functionality. In a previous project, we developed a functionality landscape (FL) hypothesis that states that 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 this project is to test this FL hypothesis. To accomplish this goal, we will achieve the following objectives by focusing on the interaction between male and female traits during the penetration of elongated genitalia and sperm storage in insects. (i) We will find causations between male/female trait properties and functionality; these causations will be explored using diverse insect groups and applying biomechanical approaches. We will find the mechanical causations of male and female sexual interactions by means of combinations of modern microscopy techniques, material distribution analyses and theoretical calculations. (ii) We will test the FL hypothesis; in particular, we will 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 genitalia and hypothetical ones to test the FL hypothesis. Furthermore, a perspective and a review paper on the FL hypothesis will be published to discuss the validity of this hypothesis. This project will provide an additional and hitherto missing perspective on genital diversification and the first concrete studies testing the universality of the theory.

• DFG Programme: Research Grants