Unique sperm haplotypes are associated with phenotypically different sperm subpopulations in Astyanax fish

Richard Borowsky, Alissa Luk, Xinjian He, Rebecca S. Kim

Research output: Contribution to journalArticle

Abstract

Background: The phenotypes of sperm are generally believed to be under the control of the diploid genotype of the male producing them rather than their own haploid genotypes, because developing spermatids share cytoplasm through intercellular bridges. This sharing is believed to homogenize their content of gene products. However, not all developing spermatids have identical gene products and estimates are that alleles at numerous gene loci are unequally expressed in sperm. This provides scope for the hypothesis that sperm phenotypes might be influenced by their unique haplotypes. Here we test a key prediction of this hypothesis. Results: The haploid hypothesis predicts that phenotypically different sperm subpopulations should be genetically distinct. We tested this by genotyping different sperm subpopulations that were generated by exposing sperm to a chemical dye challenge (Hoechst 33342). Dye treatment caused the cells to swell and tend to clump together. The three subpopulations of sperm we distinguished in flow cytometry corresponded to single cells, and clumps of two or three. Cell clumping in the presence of the dye may reflect variation in cell adhesivity. We found that allelic contents differed among the three populations. Importantly, the subpopulations with clumped sperm cells were significantly enriched in allelic combinations that had previously been observed to have significantly lower transmission success. Conclusions: We show that at least one sperm phenotype is correlated with its haploid genotype. This supports a broader hypothesis that the haploid genotypes of sperm cells may influence their fitness, with potentially significant implications for the transmission of deleterious alleles or combinations of alleles to their offspring.

Original languageEnglish (US)
Article number72
JournalBMC Biology
Volume16
Issue number1
DOIs
StatePublished - Jul 5 2018

Fingerprint

subpopulation
sperm
Fish
Haplotypes
Spermatozoa
haplotypes
Fishes
Coloring Agents
Genes
spermatozoa
fish
Haploidy
Flow cytometry
genotype
Genotype
dyes
phenotype
dye
allele
Spermatids

Keywords

  • Astyanax mexicanus
  • Cave fish
  • Sib sperm competition
  • Sperm competition
  • Sperm phenotypes

ASJC Scopus subject areas

  • Biotechnology
  • Structural Biology
  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)
  • Plant Science
  • Developmental Biology
  • Cell Biology

Cite this

Unique sperm haplotypes are associated with phenotypically different sperm subpopulations in Astyanax fish. / Borowsky, Richard; Luk, Alissa; He, Xinjian; Kim, Rebecca S.

In: BMC Biology, Vol. 16, No. 1, 72, 05.07.2018.

Research output: Contribution to journalArticle

@article{9d6c424f50bf46be8819cdbb467eecd9,
title = "Unique sperm haplotypes are associated with phenotypically different sperm subpopulations in Astyanax fish",
abstract = "Background: The phenotypes of sperm are generally believed to be under the control of the diploid genotype of the male producing them rather than their own haploid genotypes, because developing spermatids share cytoplasm through intercellular bridges. This sharing is believed to homogenize their content of gene products. However, not all developing spermatids have identical gene products and estimates are that alleles at numerous gene loci are unequally expressed in sperm. This provides scope for the hypothesis that sperm phenotypes might be influenced by their unique haplotypes. Here we test a key prediction of this hypothesis. Results: The haploid hypothesis predicts that phenotypically different sperm subpopulations should be genetically distinct. We tested this by genotyping different sperm subpopulations that were generated by exposing sperm to a chemical dye challenge (Hoechst 33342). Dye treatment caused the cells to swell and tend to clump together. The three subpopulations of sperm we distinguished in flow cytometry corresponded to single cells, and clumps of two or three. Cell clumping in the presence of the dye may reflect variation in cell adhesivity. We found that allelic contents differed among the three populations. Importantly, the subpopulations with clumped sperm cells were significantly enriched in allelic combinations that had previously been observed to have significantly lower transmission success. Conclusions: We show that at least one sperm phenotype is correlated with its haploid genotype. This supports a broader hypothesis that the haploid genotypes of sperm cells may influence their fitness, with potentially significant implications for the transmission of deleterious alleles or combinations of alleles to their offspring.",
keywords = "Astyanax mexicanus, Cave fish, Sib sperm competition, Sperm competition, Sperm phenotypes",
author = "Richard Borowsky and Alissa Luk and Xinjian He and Kim, {Rebecca S.}",
year = "2018",
month = "7",
day = "5",
doi = "10.1186/s12915-018-0538-z",
language = "English (US)",
volume = "16",
journal = "BMC Biology",
issn = "1741-7007",
publisher = "BioMed Central",
number = "1",

}

TY - JOUR

T1 - Unique sperm haplotypes are associated with phenotypically different sperm subpopulations in Astyanax fish

AU - Borowsky, Richard

AU - Luk, Alissa

AU - He, Xinjian

AU - Kim, Rebecca S.

PY - 2018/7/5

Y1 - 2018/7/5

N2 - Background: The phenotypes of sperm are generally believed to be under the control of the diploid genotype of the male producing them rather than their own haploid genotypes, because developing spermatids share cytoplasm through intercellular bridges. This sharing is believed to homogenize their content of gene products. However, not all developing spermatids have identical gene products and estimates are that alleles at numerous gene loci are unequally expressed in sperm. This provides scope for the hypothesis that sperm phenotypes might be influenced by their unique haplotypes. Here we test a key prediction of this hypothesis. Results: The haploid hypothesis predicts that phenotypically different sperm subpopulations should be genetically distinct. We tested this by genotyping different sperm subpopulations that were generated by exposing sperm to a chemical dye challenge (Hoechst 33342). Dye treatment caused the cells to swell and tend to clump together. The three subpopulations of sperm we distinguished in flow cytometry corresponded to single cells, and clumps of two or three. Cell clumping in the presence of the dye may reflect variation in cell adhesivity. We found that allelic contents differed among the three populations. Importantly, the subpopulations with clumped sperm cells were significantly enriched in allelic combinations that had previously been observed to have significantly lower transmission success. Conclusions: We show that at least one sperm phenotype is correlated with its haploid genotype. This supports a broader hypothesis that the haploid genotypes of sperm cells may influence their fitness, with potentially significant implications for the transmission of deleterious alleles or combinations of alleles to their offspring.

AB - Background: The phenotypes of sperm are generally believed to be under the control of the diploid genotype of the male producing them rather than their own haploid genotypes, because developing spermatids share cytoplasm through intercellular bridges. This sharing is believed to homogenize their content of gene products. However, not all developing spermatids have identical gene products and estimates are that alleles at numerous gene loci are unequally expressed in sperm. This provides scope for the hypothesis that sperm phenotypes might be influenced by their unique haplotypes. Here we test a key prediction of this hypothesis. Results: The haploid hypothesis predicts that phenotypically different sperm subpopulations should be genetically distinct. We tested this by genotyping different sperm subpopulations that were generated by exposing sperm to a chemical dye challenge (Hoechst 33342). Dye treatment caused the cells to swell and tend to clump together. The three subpopulations of sperm we distinguished in flow cytometry corresponded to single cells, and clumps of two or three. Cell clumping in the presence of the dye may reflect variation in cell adhesivity. We found that allelic contents differed among the three populations. Importantly, the subpopulations with clumped sperm cells were significantly enriched in allelic combinations that had previously been observed to have significantly lower transmission success. Conclusions: We show that at least one sperm phenotype is correlated with its haploid genotype. This supports a broader hypothesis that the haploid genotypes of sperm cells may influence their fitness, with potentially significant implications for the transmission of deleterious alleles or combinations of alleles to their offspring.

KW - Astyanax mexicanus

KW - Cave fish

KW - Sib sperm competition

KW - Sperm competition

KW - Sperm phenotypes

UR - http://www.scopus.com/inward/record.url?scp=85049500582&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85049500582&partnerID=8YFLogxK

U2 - 10.1186/s12915-018-0538-z

DO - 10.1186/s12915-018-0538-z

M3 - Article

C2 - 29973198

AN - SCOPUS:85049500582

VL - 16

JO - BMC Biology

JF - BMC Biology

SN - 1741-7007

IS - 1

M1 - 72

ER -