An official website of the United States government
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.
more »
« less
Nonfertilizing sperm in Lepidoptera show little evidence for recurrent positive selection
Abstract Sperm are among the most variable cells in nature. Some of this variation results from nonadaptive errors in spermatogenesis, but many species consistently produce multiple sperm morphs, the adaptive significance of which remains unknown. Here, we investigate the evolution of dimorphic sperm in Lepidoptera, the butterflies and moths. Males of this order produce both fertilizing sperm and a secondary, nonfertilizing type that lacks DNA. Previous organismal studies suggested a role for nonfertilizing sperm in sperm competition, but this hypothesis has never been evaluated from a molecular framework. We combined published data sets with new sequencing in two species, the monandrous Carolina sphinx moth and the highly polyandrous monarch butterfly. Based on population genetic analyses, we see evidence for increased adaptive evolution in fertilizing sperm, but only in the polyandrous species. This signal comes primarily from a decrease in nonsynonymous polymorphism in sperm proteins compared to the rest of the genome, suggesting stronger purifying selection, consistent with selection via sperm competition. Nonfertilizing sperm proteins, in contrast, do not show an effect of mating system and do not appear to evolve differently from the background genome in either species, arguing against the involvement of nonfertilizing sperm in direct sperm competition. Based on our results and previous work, we suggest that nonfertilizing sperm may be used to delay female remating in these insects and decrease the risk of sperm competition rather than directly affect its outcome.
more »
« less
- Award ID(s):
- 1701931
- PAR ID:
- 10457397
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 28
- Issue:
- 10
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 2517-2530
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Sperm competition is found across multicellular organisms using both external and internal fertilization. Sperm competition and post-copulatory cryptic female choice can promote incompatibility between species due to antagonistic co-evolution of the sexes within a species. This between-species incompatibility is accelerated and markedly asymmetrical when sexual mode differs, producing the “weak inbreeder, strong outcrosser” (WISO) pattern. Here, we show that male secreted short (MSS) sperm glycoproteins of nematodes constitute a gametic effector of WISO. In obligately outcrossing Caenorhabditis, MSS is dispensable for baseline fertility but required for intraspecific sperm competitiveness. MSS is lost in self-fertile lineages, likely as a response to selection for a hermaphrodite-biased sex ratio. Selfing hermaphrodites that mate with males of closely related outcrossing species are rapidly sterilized due to ovarian sperm invasion. The simplification of the male proteome in selfing species suggests many factors could contribute to invasivity. However, restoration of just MSS to the self-fertile C. briggsae is sufficient to induce mild invasivity. Further, MSS+ sperm appear to derive their competitive advantage from this behavior, directly linking interspecies incompatibility with intraspecific competition. MSS-related proteins (MSRPs) remaining in the C. briggsae genome are similar in structure, expression, and localization to MSS, but are not necessary for normal sperm competitiveness. Further, over-expression of the MSRP most similar to MSS, Cbr-MSRP-3, is insufficient to enhance competitiveness. We conclude that outcrossing species retain sperm competition factors that contribute to their reproductive isolation from selfing relatives that lost them.more » « less
-
Abstract Osteoglossiformes are an order of “bony tongue” fish considered the most primitive living order of teleosts. This review seeks to consolidate known hypotheses and identify gaps in the literature regarding the adaptive significance of diverse reproductive traits and behaviour of osteoglossiforms within the context of sperm competition and the wider lens of sexual selection. Many of the unusual traits observed in osteoglossiforms indicate low levels of sperm competition; most species have unpaired gonads, and mormyroids are the only known vertebrate species with aflagellate sperm. Several osteoglossiform families have reproductive anatomy associated with internal fertilization but perform external fertilization, which may be representative of the evolutionary transition from external to internal fertilization and putative trade‐offs between sperm competition and the environment. They also employ every type of parental care seen in vertebrates. Geographically widespread and basally situated within teleosts, osteoglossiforms present an effective study system for understanding how sperm competition and sexual selection have shaped the evolution of teleost reproductive behaviour, sperm and gonad morphology, fertilization strategies, courtship and paternal care, and sexual conflict. The authors suggest that the patterns seen in osteoglossiform reproduction are a microcosm of teleost reproductive diversity, potentially signifying the genetic plasticity that contributed to the adaptive radiation of teleost fishes.more » « less
-
Abstract It remains unclear how variation in the intensity of sperm competition shapes phenotypic and molecular evolution across clades. Mice and rats in the subfamily Murinae are a rapid radiation exhibiting incredible diversity in sperm morphology and production. We combined phenotypic and genomic data to perform phylogenetic comparisons of male reproductive traits and genes across 78 murine species. We identified several shifts towards smaller relative testes mass (RTM), presumably reflecting reduced sperm competition. Several sperm traits were associated with RTM, suggesting that mating system evolution selects for convergent suites of traits related to sperm competitive ability. We predicted that sperm competition would also drive more rapid molecular divergence in species with large testes. Contrary to this, we found that many spermatogenesis genes evolved more rapidly in species with smaller RTM due to relaxed purifying selection. While some reproductive genes evolved rapidly under recurrent positive selection, relaxed selection played a greater role in underlying rapid evolution in small testes species. Our work demonstrates that postcopulatory sexual selection can impose strong purifying selection shaping the evolution of male reproduction and that broad patterns of molecular evolution may help identify genes that contribute to male fertility.more » « less
-
Abstract Successful reproduction depends on interactions between numerous proteins beyond those involved directly in gamete fusion. Although such reproductive proteins evolve in response to sexual selection pressures, how networks of interacting proteins arise and evolve as reproductive phenotypes change remains an open question. Here, we investigated the molecular evolution of the ‘sex peptide network’ ofDrosophila melanogaster,a functionally well‐characterized reproductive protein network. In this species, the peptide hormone sex peptide (SP) and its interacting proteins cause major changes in female physiology and behaviour after mating. In contrast, females of more distantly relatedDrosophilaspecies do not respond to SP. In spite of these phenotypic differences, we detected orthologs of all network proteins across 22 diverseDrosophilaspecies and found evidence that most orthologs likely function in reproduction throughout the genus. Within SP‐responsive species, we detected the recurrent, adaptive evolution of several network proteins, consistent with sexual selection acting to continually refine network function. We also found some evidence for adaptive evolution of several proteins along two specific phylogenetic lineages that correspond with increased expression of the SP receptor in female reproductive tracts or increased sperm length, respectively. Finally, we used gene expression profiling to examine the likely degree of functional conservation of the paralogs of an SP network protein that arose via gene duplication. Our results suggest a dynamic history for the SP network in which network members arose before the onset of robust SP‐mediated responses and then were shaped by both purifying and positive selection.more » « less
