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.
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Nonfertilizing sperm in Lepidoptera show little evidence for recurrent positive selection
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
- NSF-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
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Abstract Sperm cells of all taxa share a common goal to reach and fertilize an ovum, yet sperm are one of the most diverse cell types in nature. While the structural diversity of these cells is well recognized, the functional significance of variation in sperm design remains elusive. An important function of spermatozoa is a need to migrate toward the ova, often over long distances in a foreign environment, which may include a complex and hostile female reproductive tract. Several comparative and experimental studies have attempted to address the link between sperm morphology and motility, yet the conclusions drawn from these studies are often inconsistent, even within the same taxa. Much of what we know about the functional significance of sperm design in internally fertilizing species has been gleaned from in vitro studies, for which experimental parameters often vary among studies. We propose that discordant results from these studies are in part due to a lack of consistency of methods, conditions that do not replicate those of the female reproductive tract, and the overuse of simple linear measures of sperm shape. Within this review, we provide a toolkit for imaging, quantifying, and analyzing sperm morphology and movement patterns for in vitro studies and discuss emerging approaches. Results from studies linking morphology to motility enhance our understanding of the evolution of adaptive sperm traits and the mechanisms that regulate fertility, thus offering new insights into methods used in assisted reproductive technologies in animal science, conservation and public health.
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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’ of
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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.
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Premise Male gametophytes of most seed plants deliver sperm to eggs via a pollen tube. Pollen tube growth rates (
PTGR s) of angiosperms are exceptionally rapid, a pattern attributed to more effective haploid selection under stronger pollen competition. Paradoxically, whole genome duplication (WGD ) has been common in angiosperms but rare in gymnosperms. Pollen tube polyploidy should initially acceleratePTGR because increased heterozygosity and gene dosage should increase metabolic rates. However, polyploidy should also independently increase tube cell size, causing more work which should decelerate growth. We asked how genome size changes have affected the evolution of seed plantPTGR s.Methods We assembled a phylogenetic tree of 451 species with known
PTGR s. We then used comparative phylogenetic methods to detect effects of neo‐polyploidy (within‐genus origins),DNA content, andWGD history onPTGR , and correlated evolution ofPTGR andDNA content.Results Gymnosperms had significantly higher
DNA content and slowerPTGR optima than angiosperms, and theirPTGR andDNA content were negatively correlated. For angiosperms, 89% of model weight favored Ornstein‐Uhlenbeck models with a fasterPTGR optimum for neo‐polyploids, whereasPTGR andDNA content were not correlated. For within‐genus and intraspecific‐cytotype pairs,PTGR s of neo‐polyploids < paleo‐polyploids.Conclusions Genome size increases should negatively affect
PTGR when genetic consequences ofWGD s are minimized, as found in intra‐specific autopolyploids (low heterosis) and gymnosperms (fewWGD s). But in angiosperms, the higherPTGR optimum of neo‐polyploids and non‐negativePTGR ‐DNA content correlation suggest that recurrentWGD s have caused substantialPTGR evolution in a non‐haploid state.
