Male phenotypes in a female framework: Evidence for degeneration in sperm produced by male snails from asexual lineages

Jalinsky, Joseph; Logsdon, John M.; Neiman, Maurine

doi:10.1111/jeb.13632

Cited by 20 publications

(24 citation statements)

References 60 publications

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Section: Discussionsupporting

confidence: 92%

“…Evolutionary decay of mating-related traits in asexual contexts is a plausible explanation for these results and is consistent with a previous study demonstrating evidence for decay of sperm traits in the male offspring occasionally produced by asexual female P. antipodarum [15]. Despite absence of evidence for discriminatory mating behaviour, asexual females mated at a nearly identical frequency with P. antipodarum males as sexual females (Fig.…”

Section: Discussionsupporting

confidence: 92%

“…The copyright holder for this preprint (which this version posted June 9, 2021. ; https://doi.org/10.1101/2021.06.08.447504 doi: bioRxiv preprint do not outweigh the benefits of trait maintenance [13,14]. Several studies have supported these ideas, finding abnormal or fully decayed traits involved in mating and reproduction (spermathecae in asexual Timema stick insects [13]; sperm in asexual P. antipodarum males [15]) in asexual organisms. These results suggest that these traits are not being maintained by selection, at least to the extent of the same traits in sexual counterparts.…”

Section: Introductionmentioning

confidence: 99%

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Asexual freshwater snails make poor mate choice decisions

Stork

Jalinsky

Neiman

2021

Preprint

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Once-useful traits that no longer contribute to fitness tend to decay over time. We address whether the expression of mating-related traits that increase the fitness of sexually reproducing individuals but are likely less useful or even costly to asexual counterparts seems to exhibit decay in the latter. Potamopyrgus antipodarum is a New Zealand freshwater snail characterized by repeated transitions from sexual to asexual reproduction. The frequent coexistence of sexual and asexual lineages makes P. antipodarum an excellent model for the study of mating-related trait loss. We used a mating choice assay including sexual and asexual P. antipodarum females and conspecific (presumed better choice) vs. heterospecific (presumed worse choice) males to evaluate the loss of behavioural traits related to sexual reproduction. We found that sexual females engaged in mating behaviours with conspecific mating partners more frequently and for a greater duration than with heterospecific mating partners, while asexual females seemed to lack the ability to make a choice. These results suggest that selection acting to maintain mate choice in asexual P. antipodarum is weak or ineffective relative to sexual females and that asexual reproduction likely contributes to the evolutionary decay of behavioural traits in this system.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Asexual freshwater snails make poor mate choice decisions

Stork

Jalinsky

Neiman

2021

Preprint

Self Cite

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“…At one extreme, the pairing of JU1373 hermaphrodites from Réunion with JU1630 males from Cape Verde yielded no cross-progeny from 22 trials, while at the other extreme, Hawaiian QG131 hermaphrodites and South American NIC58 males yielded cross-progeny in each of 34 trials. Male crossing probability was much more variable than that of hermaphrodites, consistent with relaxed selection (residual deviance of 179.2 vs. 85.2, null deviance 232.6, binomial linear model) ( Cutter, 2019 ; Jalinsky et al, 2020 ; Noble et al, 2015 ; Palopoli et al, 2008 ; van der Kooi and Schwander, 2014 ). Same-strain pairings were indistinguishable from inter-strain pairings (p=0.88, likelihood ratio test [LRT] of binomial linear models).…”

Section: Resultsmentioning

confidence: 56%

Selfing is the safest sex for Caenorhabditis tropicalis

Noble

Yuen

Stevens

et al. 2021

eLife

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Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, Caenorhabditis tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple Medea-like elements, genetically consistent with maternal toxin/zygotic antidote systems. Loci with Medea activity harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating Medea elements dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid Medea-mediated outbreeding depression.

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“…Among the focal Peromyscus species within our study, we found more variation in the sperm head aspect ratio and head width across than within species, with some species producing sperm with a relatively wider head (P. eremicus, P. polionotus, and P. maniculatus) and others producing a more elongated head (P. californicus, P. leucopus, and P. gossypinus). The elongation of the sperm head, driven by the compactness of the nucleus within [59][60][61][62][63][64] is expected to reduce hydrodynamic drag and promote more efficient, faster movements [16, but see 15]. Sperm head shape has been observed in both inter-and intra-species analyses across taxonomic groups [17][18][19][21][22][23], but see 65,66].…”

Section: Discussionmentioning

confidence: 99%

The social shape of sperm: Using an integrative machine-learning approach to examine sperm ultrastructure and collective motility

Hook

Yang

Campanello

et al. 2020

Preprint

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Sperm are one of the most morphologically diverse cell types in nature, yet they also exhibit remarkable behavioral variation, including the formation of collective groups of cells that swim together for motility or transport through the female reproductive tract. Here we take advantage of the natural variation in sperm traits observed across Peromyscus mice to test the hypothesis that the morphology of the rodent sperm head influences their sperm aggregation behavior. Using machine learning and traditional morphometric approaches to quantify and analyze their complex shapes, we show that the elongation of the sperm head is the most distinguishing morphological trait in these rodents and, as predicted, significantly associates with collective sperm movements obtained from in vitro observations. We then successfully use neural network analysis to predict the size and proportion of sperm aggregates from sperm head morphology and show that species whose sperm feature relatively wider heads aggregate more often and form larger groups, providing support for the theoretical prediction that an adhesive region around the equatorial region of the sperm head mediates these unique gametic interactions. Together these findings advance our understanding of how even subtle variation in sperm design can drive differences in sperm function and performance.Subject AreasEvolution, Cellular Biology, Behavior

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Male phenotypes in a female framework: Evidence for degeneration in sperm produced by male snails from asexual lineages

Abstract: This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as

Cited by 20 publications

References 60 publications

Asexual freshwater snails make poor mate choice decisions

Asexual freshwater snails make poor mate choice decisions

Selfing is the safest sex for Caenorhabditis tropicalis

The social shape of sperm: Using an integrative machine-learning approach to examine sperm ultrastructure and collective motility

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