Male fertility advantage within and between seasons in the perennial androdioecious plant Phillyrea angustifolia.

Phillyrea angustifolia androdioecy flowering rhythmicity male advantage multistate capture-recapture model perennial plants reproductive systems

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
01 Nov 2023
Historique:
received: 26 10 2023
medline: 6 11 2023
pubmed: 6 11 2023
entrez: 6 11 2023
Statut: aheadofprint

Résumé

Androdioecy, the co-occurrence of males and hermaphrodites, is a rare reproductive system. Males can be maintained if they benefit from a higher male fitness than hermaphrodites, referred to as male advantage. Male advantage may emerge from increased fertility due to resource reallocation. However, empirical studies usually compare sexual phenotypes over a single flowering season, thus ignoring potential cumulative effects over successive seasons in perennials. In this study, we quantify various components of male fertility advantage both within and between seasons in the long-lived perennial shrub Phillyrea angustifolia (Oleaceae). While, owing to a peculiar diallelic self-incompatibility system and female sterility mutation strictly associated with a breakdown of incompatibility, males do not need fertility advantage to persist in this species, this advantage remains an important determinant of their equilibrium frequency. A survey of more than 1000 full-sib plants allowed us to compare males and hermaphrodites for several components of male fertility. Individuals were characterized for proxies of pollen production and vegetative growth. By analyzing maternal progenies, we compared the siring success of males and hermaphrodites. Finally, we assessed for each sexual morph how the intensity of flowering on one year impacts next-year growth and reproduction using multistate capture-recapture model. Males benefited from a greater vegetative growth and flowering intensity. Within one season, males sired twice as many seeds as equidistant, compatible hermaphroditic competitors. In addition, males more often maintained intense flowering over successive years. Finally, investment in male reproductive function appeared to differ between the two incompatibility groups of hermaphrodites. Males, by sparing the cost of female reproduction, have a higher flowering frequency and vegetative growth, which both contribute to male advantage over individual lifetime. This suggests that studies analyzing sexual phenotypes only during single reproductive periods likely provide inadequate estimates of male advantage in perennials.

Sections du résumé

BACKGROUND AND AIMS OBJECTIVE
Androdioecy, the co-occurrence of males and hermaphrodites, is a rare reproductive system. Males can be maintained if they benefit from a higher male fitness than hermaphrodites, referred to as male advantage. Male advantage may emerge from increased fertility due to resource reallocation. However, empirical studies usually compare sexual phenotypes over a single flowering season, thus ignoring potential cumulative effects over successive seasons in perennials. In this study, we quantify various components of male fertility advantage both within and between seasons in the long-lived perennial shrub Phillyrea angustifolia (Oleaceae). While, owing to a peculiar diallelic self-incompatibility system and female sterility mutation strictly associated with a breakdown of incompatibility, males do not need fertility advantage to persist in this species, this advantage remains an important determinant of their equilibrium frequency.
METHODS METHODS
A survey of more than 1000 full-sib plants allowed us to compare males and hermaphrodites for several components of male fertility. Individuals were characterized for proxies of pollen production and vegetative growth. By analyzing maternal progenies, we compared the siring success of males and hermaphrodites. Finally, we assessed for each sexual morph how the intensity of flowering on one year impacts next-year growth and reproduction using multistate capture-recapture model.
KEY RESULTS RESULTS
Males benefited from a greater vegetative growth and flowering intensity. Within one season, males sired twice as many seeds as equidistant, compatible hermaphroditic competitors. In addition, males more often maintained intense flowering over successive years. Finally, investment in male reproductive function appeared to differ between the two incompatibility groups of hermaphrodites.
CONCLUSION CONCLUSIONS
Males, by sparing the cost of female reproduction, have a higher flowering frequency and vegetative growth, which both contribute to male advantage over individual lifetime. This suggests that studies analyzing sexual phenotypes only during single reproductive periods likely provide inadequate estimates of male advantage in perennials.

Identifiants

pubmed: 37930793
pii: 7335570
doi: 10.1093/aob/mcad169
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Auteurs

F Laugier (F)

CEFE, Univ Montpellier, CNRS, Univ Paul Valery Montpellier, EPHE, IRD, Montpellier, France.

P Saumitou-Laprade (P)

Univ. Lille, CNRS, UMR 8198 - Evo-Eco-Paleo, F-59000 Lille, France.

P Vernet (P)

Univ. Lille, CNRS, UMR 8198 - Evo-Eco-Paleo, F-59000 Lille, France.

J Lepart (J)

CEFE, Univ Montpellier, CNRS, Univ Paul Valery Montpellier, EPHE, IRD, Montpellier, France.

P-O Cheptou (PO)

CEFE, Univ Montpellier, CNRS, Univ Paul Valery Montpellier, EPHE, IRD, Montpellier, France.

M Dufay (M)

CEFE, Univ Montpellier, CNRS, Univ Paul Valery Montpellier, EPHE, IRD, Montpellier, France.

Classifications MeSH