Evolutionary Proteomics Reveals Distinct Patterns of Complexity and Divergence between Lepidopteran Sperm Morphs

Emma Whittington, Timothy L. Karr, Andrew J. Mongue, Steve Dorus, James R. Walters

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Spermatozoa are one of the most strikingly diverse animal cell types. One poorly understood example of this diversity is sperm heteromorphism, where males produce multiple distinct morphs of sperm in a single ejaculate. Typically, only one morph is capable of fertilization and the function of the nonfertilizing morph, called parasperm, remains to be elucidated. Sperm heteromorphism has multiple independent origins, including Lepidoptera (moths and butterflies), where males produce a fertilizing eupyrene sperm and an apyrene parasperm, which lacks a nucleus and nuclear DNA. Here we report a comparative proteomic analysis of eupyrene and apyrene sperm between two distantly related lepidopteran species, the monarch butterfly (Danaus plexippus) and Carolina sphinx moth (Manduca sexta). In both species, we identified ∼700 sperm proteins, with half present in both morphs and the majority of the remainder observed only in eupyrene sperm. Apyrene sperm thus have a distinctly less complex proteome. Gene ontology (GO) analysis revealed proteins shared between morphs tend to be associated with canonical sperm cell structures (e.g., flagellum) and metabolism (e.g., ATP production). GO terms for morph-specific proteins broadly reflect known structural differences, but also suggest a role for apyrene sperm in modulating female neurobiology. Comparative analysis indicates that proteins shared between morphs are most conserved between species as components of sperm, whereas morph-specific proteins turn over more quickly, especially in apyrene sperm. The rapid divergence of apyrene sperm content is consistent with a relaxation of selective constraints associated with fertilization and karyogamy. On the other hand, parasperm generally exhibit greater evolutionary lability, and our observations may therefore reflect adaptive responses to shifting regimes of sexual selection.

Original languageEnglish (US)
Pages (from-to)1838-1846
Number of pages9
JournalGenome biology and evolution
Volume11
Issue number7
DOIs
StatePublished - Jul 1 2019
Externally publishedYes

Fingerprint

proteomics
morphs
sperm
Proteomics
Spermatozoa
divergence
Lepidoptera
spermatozoa
protein
Danaus plexippus
Butterflies
Gene Ontology
Moths
butterfly
lepidopteran
Proteins
moth
Fertilization
proteins
Manduca

Keywords

  • apyrene sperm
  • eupyrene sperm
  • fertility
  • parasperm
  • sexual selection
  • spermatogenesis

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Evolutionary Proteomics Reveals Distinct Patterns of Complexity and Divergence between Lepidopteran Sperm Morphs. / Whittington, Emma; Karr, Timothy L.; Mongue, Andrew J.; Dorus, Steve; Walters, James R.

In: Genome biology and evolution, Vol. 11, No. 7, 01.07.2019, p. 1838-1846.

Research output: Contribution to journalArticle

Whittington, Emma ; Karr, Timothy L. ; Mongue, Andrew J. ; Dorus, Steve ; Walters, James R. / Evolutionary Proteomics Reveals Distinct Patterns of Complexity and Divergence between Lepidopteran Sperm Morphs. In: Genome biology and evolution. 2019 ; Vol. 11, No. 7. pp. 1838-1846.
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