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

Citation

Gomez, R Antonio; Maddison, David (2020), Novelty and emergent patterns in sperm: morphological diversity and evolution of spermatozoa and sperm conjugation in ground beetles (Coleoptera: Carabidae), Dryad, Dataset, https://doi.org/10.5061/dryad.7m0cfxpqt

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.

Methods

These data include sperm data recorded for 177 species of the beetle family Carabidae, trees dervied from a low-resolution phylogeny of the group, R scripts and data, and online supporting information.

The sperm data was collected from live beetles using light microscopy and image analysis. The trees were derived from the literature and software programs designed for evolutionary analyses (Mesquite and R).

The data were analyzed using a comparative phylogenetic framework using various R packages.

Usage Notes

Supplemental figure


  • Figure S1 SuppInfo.pdf (a sperm conjugate morphospace for 55 species of ground beetles showing trait loadings for PC1 and PC2)

 

Media


16 movies of carabid sperm of 8 different species viewed in saline on slides

 

Methods S1 SuppInfo.docx


Supplemental methods describing additional details of our methods for sperm data collection

 

R data


Various data files used for comparative analyses in R

  • 1000trees.phy (1000 fully dichotomous random resolutions of our low-resolution phylogeny of Carabidae in phylip format)
  • colors.txt (a text file with discrete conjugation type data for carabid beetles for use in plotting)
  • ConjugateDataCarabidR.txt (a text file containing continouous trait data for our studied conjugate traits across carabid beetles)
  • discretetraitsRdata.txt (a text file containing discrete character data for carabid beetles)
  • JustSpermDataCarabidR.txt (a text file containing continuous trait data for our studied sperm traits across carabid beetles)
  • Species.Pairs.Data.txt (a text file containing the quotients of species traits values for 7 continouous sperm traits between 20 species pairs of ground beetles)
  • SpermDataCarabid.nex (a nexus file for Mesquite containing our low-resolution phylogeny and 7 continous sperm trait data for 177 species of ground beetles)
  • SpermDataCarabid.phy (a low-resolution phylogeny of Carabidae in phylip format with branch lengths arbitrarily ultrametricized in Mesquite)
  • SpermDataCarabidR.txt (a text file containing continuous trait data for our 7 continuous sperm traits across carabid beetles)

 

R scripts


  • CompareUnivariateModels.2.2.R (R script that fits several models of evolution for sperm head length and the number of sperm in a conjugate using phytools function make.simmap to reconstruct ancestral regimes and OUwie for model fitting and data simulation)
  • construct.morphospace.1.0.R (R script for reconstructing sperm phylomorphospaces for 101 species of ground beetles and a morphospace of all studied sperm data for 55 species of ground beetles)
  • pANOVA.PGLS.spermtraits.1.0.R (R script for performing pANOVAs and PGLS on ground beetle sperm data)
  • Species.Pairs.Comparison.1.0.R (R script that performs a one-way ANOVA and a post-hoc Tukey HSD test of sperm and conjugate data for 20 species pairs of ground beeltes)
  • StochasticMaps.2.0.R (R script that performs ancestral character estimation using stochastic character mapping of conjugate type data for ground beetles using various sets of trees with different branch length schemes)

 

Spreadsheet S1 SuppInfo.xslx


Excel spreadsheet with sperm trait data recorded for 397 specimens of ground beetles.

 

Supplemental References Cited SuppInfo.docx


Microsoft word document containing our supplemental references cited

 

Table S1 SuppInfo.docx


A supplemental table containing data summarizing the state of knowledge of ground beetle sperm phenotype.

 

Table S2 SuppInfo.docx


A supplemental table containing taxon and specimen sampling for sperm data.

 

Table S3 SuppInfo.docx


A supplemental table containing data locality data of studied specimens.

 

Table S4 SuppInfo.docx


A supplemental table containing sperm data summarized across specimens for 177 species of ground beetles.

 

Table S5 SuppInfo.docx


A supplemental table containing results of a one-way ANOVA of data for 20 species pairs of ground beetles recorded for all 7 studied continuous traits.

 

Taxon-by-taxon results S1 SuppInfo.docx


Supplemental results containing detailed taxon-by-taxon observations of sperm taken from this study and the literature.

 

Funding

NSF, Award: DGE-1143953

Oregon State University, Award: Harold E. and Leona M. Rice Endowment Fund