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Novelty and emergent patterns in sperm: morphological diversity and evolution of spermatozoa and sperm conjugation in ground beetles (Coleoptera: Carabidae)

Gomez, R Antonio1; Maddison, David1

Published Mar 13, 2020 on Dryad. https://doi.org/10.5061/dryad.7m0cfxpqt

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Mar 13, 2020 version files 72.68 MB

Abstract

The beetle family Carabidae, with about 40,000 species, exhibits enough diversity in sperm structure and behavior to be an excellent model system for studying patterns and processes of sperm evolution. We explore their potential, documenting sperm form in 177 species of ground beetles using light microscopy and collecting data on 1 qualitative and 7 quantitative sperm phenotypic traits. Our sampling captures 61% of the tribal-level diversity of ground beetles. These data highlight the notable morphological diversity of sperm in ground beetles and suggest that sperm in the group have dynamic evolutionary histories with much morphological innovation and convergence. Sperm vary among species in total length (48–3,400mm), head length (0.5–270mm), and head width (0.2–6.3mm). Most ground beetles make sperm with heads that are indistinct from the flagella at the gross morphological level. However, some or all Omophron,Trachypachus, and Dyschiriini make broad-headed sperm that show morphological differences between species. Most ground beetles package their sperm into groups of sperm, termed conjugates, and ground beetles show variation in conjugate form and in the number and arrangement of sperm in a conjugate. Most ground beetles make sperm conjugates by embedding their sperm in a hyaline rod or spermatostyle. The spermatostyle is remarkably variable among species and varies in length from 17–41,000mm. Several unrelated groups of ground beetles make only singleton sperm, including Nebriinae, Cicindelinae, many Trechinae, and the tribe Paussini. In order to study patterns in sperm evolution, we combine these data with a low-resolution phylogeny of ground beetles. Results from modern comparative analyses suggest the following: sperm differ from conjugates in some aspect of their underlying evolutionary process, sperm have influenced conjugate evolution and vice versa, and conjugation with a spermatostyle likely evolved early within the history of Carabidae and it has been lost independently at least three times.