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

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.