Plant-like mating in an animal:sexual compatibility and allocation trade-offs in a simultaneous hermaphrodite with remote transfer of sperm

A. J. Pemberton, A. D. Sommerfeldt, C. A. Wood, H. C. Flint, Leslie Robert Noble, K. R. Clarke, J. D. D. Bishop

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

The importance of sexual compatibility between mates has only recently been realized in zoological research into sexual selection, yet its study has been central to botanical research for many decades. The reproductive characteristics of remote mating, an absence of precopulatory mate screening, internal fertilization and embryonic brooding are shared between passively pollinated plants and a phylogenetically diverse group of sessile aquatic invertebrates. Here, we further characterize the sexual compatibility system of one such invertebrate, the colonial ascidian Diplosoma listerianum. All 66 reciprocal pairings of 12 genetic individuals were carried out. Fecundities of crosses varied widely and suggested a continuous scale of sexual compatibility. Of the 11 animals from the same population c. 40% of crosses were completely incompatible with a further c. 20% having obvious partial compatibility (reduced fecundity). We are unaware of other studies documenting such high levels of sexual incompatibility in unrelated individuals. RAPD fingerprinting was used to estimate relatedness among the 12 individuals after a known pedigree was successfully reconstructed to validate the technique. in contrast to previous results, no correlation between genetic similarity and sexual compatibility was detected. The blocking of many genotypes of sperm is expected to severely modify realized paternity away from 'fair raffle' expectations and probably reduce levels of intra-brood genetic diversity in this obligatorily promiscuous mating system. One adaptive benefit may be to reduce the bombardment of the female reproductive system by outcrossed sperm with conflicting evolutionary interests, so as to maintain female control of somatic : gametic investment.

Original languageEnglish
Pages (from-to)506-518
Number of pages12
JournalJournal of Evolutionary Biology
Volume17
Issue number3
DOIs
Publication statusPublished - May 2004

Keywords

  • allocation
  • brooding
  • Diplosoma listerianum
  • fertilization
  • genetic incompatibility
  • sexual compatibility
  • simultaneous hermaphrodite
  • spermcast
  • trade-off
  • ASCIDIAN DIPLOSOMA-LISTERIANUM
  • LIFE-HISTORY VARIATION
  • WATER-BORNE SPERM
  • BRYOZOAN CELLEPORELLA-HYALINA
  • REPRODUCTIVE SUCCESS
  • BOTRYLLUS-SCHLOSSERI
  • FEMALE CONTROL
  • SELECTION
  • COMPETITION
  • POPULATION

Cite this

Plant-like mating in an animal:sexual compatibility and allocation trade-offs in a simultaneous hermaphrodite with remote transfer of sperm. / Pemberton, A. J.; Sommerfeldt, A. D.; Wood, C. A.; Flint, H. C.; Noble, Leslie Robert; Clarke, K. R.; Bishop, J. D. D.

In: Journal of Evolutionary Biology, Vol. 17, No. 3, 05.2004, p. 506-518.

Research output: Contribution to journalArticle

Pemberton, A. J. ; Sommerfeldt, A. D. ; Wood, C. A. ; Flint, H. C. ; Noble, Leslie Robert ; Clarke, K. R. ; Bishop, J. D. D. / Plant-like mating in an animal:sexual compatibility and allocation trade-offs in a simultaneous hermaphrodite with remote transfer of sperm. In: Journal of Evolutionary Biology. 2004 ; Vol. 17, No. 3. pp. 506-518.
@article{d30ca3a6c21d43b1a897b4396ff81954,
title = "Plant-like mating in an animal:sexual compatibility and allocation trade-offs in a simultaneous hermaphrodite with remote transfer of sperm",
abstract = "The importance of sexual compatibility between mates has only recently been realized in zoological research into sexual selection, yet its study has been central to botanical research for many decades. The reproductive characteristics of remote mating, an absence of precopulatory mate screening, internal fertilization and embryonic brooding are shared between passively pollinated plants and a phylogenetically diverse group of sessile aquatic invertebrates. Here, we further characterize the sexual compatibility system of one such invertebrate, the colonial ascidian Diplosoma listerianum. All 66 reciprocal pairings of 12 genetic individuals were carried out. Fecundities of crosses varied widely and suggested a continuous scale of sexual compatibility. Of the 11 animals from the same population c. 40{\%} of crosses were completely incompatible with a further c. 20{\%} having obvious partial compatibility (reduced fecundity). We are unaware of other studies documenting such high levels of sexual incompatibility in unrelated individuals. RAPD fingerprinting was used to estimate relatedness among the 12 individuals after a known pedigree was successfully reconstructed to validate the technique. in contrast to previous results, no correlation between genetic similarity and sexual compatibility was detected. The blocking of many genotypes of sperm is expected to severely modify realized paternity away from 'fair raffle' expectations and probably reduce levels of intra-brood genetic diversity in this obligatorily promiscuous mating system. One adaptive benefit may be to reduce the bombardment of the female reproductive system by outcrossed sperm with conflicting evolutionary interests, so as to maintain female control of somatic : gametic investment.",
keywords = "allocation, brooding, Diplosoma listerianum, fertilization, genetic incompatibility, sexual compatibility, simultaneous hermaphrodite, spermcast, trade-off, ASCIDIAN DIPLOSOMA-LISTERIANUM, LIFE-HISTORY VARIATION, WATER-BORNE SPERM, BRYOZOAN CELLEPORELLA-HYALINA, REPRODUCTIVE SUCCESS, BOTRYLLUS-SCHLOSSERI, FEMALE CONTROL, SELECTION, COMPETITION, POPULATION",
author = "Pemberton, {A. J.} and Sommerfeldt, {A. D.} and Wood, {C. A.} and Flint, {H. C.} and Noble, {Leslie Robert} and Clarke, {K. R.} and Bishop, {J. D. D.}",
year = "2004",
month = "5",
doi = "10.1111/j.1420-9101.2004.00708.x",
language = "English",
volume = "17",
pages = "506--518",
journal = "Journal of Evolutionary Biology",
issn = "1010-061X",
publisher = "Wiley-Blackwell",
number = "3",

}

TY - JOUR

T1 - Plant-like mating in an animal:sexual compatibility and allocation trade-offs in a simultaneous hermaphrodite with remote transfer of sperm

AU - Pemberton, A. J.

AU - Sommerfeldt, A. D.

AU - Wood, C. A.

AU - Flint, H. C.

AU - Noble, Leslie Robert

AU - Clarke, K. R.

AU - Bishop, J. D. D.

PY - 2004/5

Y1 - 2004/5

N2 - The importance of sexual compatibility between mates has only recently been realized in zoological research into sexual selection, yet its study has been central to botanical research for many decades. The reproductive characteristics of remote mating, an absence of precopulatory mate screening, internal fertilization and embryonic brooding are shared between passively pollinated plants and a phylogenetically diverse group of sessile aquatic invertebrates. Here, we further characterize the sexual compatibility system of one such invertebrate, the colonial ascidian Diplosoma listerianum. All 66 reciprocal pairings of 12 genetic individuals were carried out. Fecundities of crosses varied widely and suggested a continuous scale of sexual compatibility. Of the 11 animals from the same population c. 40% of crosses were completely incompatible with a further c. 20% having obvious partial compatibility (reduced fecundity). We are unaware of other studies documenting such high levels of sexual incompatibility in unrelated individuals. RAPD fingerprinting was used to estimate relatedness among the 12 individuals after a known pedigree was successfully reconstructed to validate the technique. in contrast to previous results, no correlation between genetic similarity and sexual compatibility was detected. The blocking of many genotypes of sperm is expected to severely modify realized paternity away from 'fair raffle' expectations and probably reduce levels of intra-brood genetic diversity in this obligatorily promiscuous mating system. One adaptive benefit may be to reduce the bombardment of the female reproductive system by outcrossed sperm with conflicting evolutionary interests, so as to maintain female control of somatic : gametic investment.

AB - The importance of sexual compatibility between mates has only recently been realized in zoological research into sexual selection, yet its study has been central to botanical research for many decades. The reproductive characteristics of remote mating, an absence of precopulatory mate screening, internal fertilization and embryonic brooding are shared between passively pollinated plants and a phylogenetically diverse group of sessile aquatic invertebrates. Here, we further characterize the sexual compatibility system of one such invertebrate, the colonial ascidian Diplosoma listerianum. All 66 reciprocal pairings of 12 genetic individuals were carried out. Fecundities of crosses varied widely and suggested a continuous scale of sexual compatibility. Of the 11 animals from the same population c. 40% of crosses were completely incompatible with a further c. 20% having obvious partial compatibility (reduced fecundity). We are unaware of other studies documenting such high levels of sexual incompatibility in unrelated individuals. RAPD fingerprinting was used to estimate relatedness among the 12 individuals after a known pedigree was successfully reconstructed to validate the technique. in contrast to previous results, no correlation between genetic similarity and sexual compatibility was detected. The blocking of many genotypes of sperm is expected to severely modify realized paternity away from 'fair raffle' expectations and probably reduce levels of intra-brood genetic diversity in this obligatorily promiscuous mating system. One adaptive benefit may be to reduce the bombardment of the female reproductive system by outcrossed sperm with conflicting evolutionary interests, so as to maintain female control of somatic : gametic investment.

KW - allocation

KW - brooding

KW - Diplosoma listerianum

KW - fertilization

KW - genetic incompatibility

KW - sexual compatibility

KW - simultaneous hermaphrodite

KW - spermcast

KW - trade-off

KW - ASCIDIAN DIPLOSOMA-LISTERIANUM

KW - LIFE-HISTORY VARIATION

KW - WATER-BORNE SPERM

KW - BRYOZOAN CELLEPORELLA-HYALINA

KW - REPRODUCTIVE SUCCESS

KW - BOTRYLLUS-SCHLOSSERI

KW - FEMALE CONTROL

KW - SELECTION

KW - COMPETITION

KW - POPULATION

U2 - 10.1111/j.1420-9101.2004.00708.x

DO - 10.1111/j.1420-9101.2004.00708.x

M3 - Article

VL - 17

SP - 506

EP - 518

JO - Journal of Evolutionary Biology

JF - Journal of Evolutionary Biology

SN - 1010-061X

IS - 3

ER -