A novel sexual system in male gametophytes of Laminaria pallida (Phaeophyceae)

ABSTRACT

Brown algae (Phaeophyceae) exhibit a wide diversity of sexual systems, reproductive modes and life histories. The evolution of this diversity has often involved transitions between sexual systems, which may influence genetic diversity and diversification, and phenotypic evolution. This study reports a novel sexual system in kelp. We identified male gametophyte strains of Laminaria pallida that, despite presenting morphological features typical of a male, developed both antheridia and egg-like structures, which suggest an incomplete suppression of femaleness during sexual determination of gametophytes. The sperm released by these variant male gametophytes successfully fertilize eggs produced by female gametophytes, developing into sporophytes with normal morphologies. However, morphologically abnormal sporophytic offspring were formed in isolated variant male gametophytes, indicating that the egg-like structures were not successfully self-fertilized by sperm. The causes of the unsuccessful intragametophytic selfing are unknown, but absence of pheromone production by the egg-like structures is a hypothesis suggested by available evidence. Partial co-sexuality is clearly inherited, as all male gametophyte strains descended from the same sporophyte developed egg-like structures. Further investigation into the genetics and maturation of male partheno-sporophytes will help to estimate the potential effects of this mechanism on natural populations.

Highlights

• Morphologically typical male gametophytes in Laminaria pallida developed both antheridia and egg-like structures.

• Male sexual reproductive ability was retained by partially co-sexual L. pallida gametophytes.

• Partial co-sexuality appears to be heritable but varies between L. pallida individuals.

KEYWORDS:

• Brown alga
• development
• monoicy
• parthenogenesis
• sexual system
• sporophyte formation

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary information

The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2024.2314487

Supplementary figure S1. Development of gametogenesis stages in different control male gametophyte strains of Laminaria pallida derived from sporophytes C, D and F after 20 days in gametogenic conditions when isolated. 100% stacked column charts with means of each ontogenetic stage (n = 4). SE values are omitted for clarity.

Supplementary figure S2. Morphological characterization of control male gametophytes of Laminaria pallida derived from sporophytes C (picture A), F (B) and D (C). All gametophytes show antheridia (arrows), but no egg-like structure or partheno-sporophytes. Scale bars: 100 μm.

Author contributions

P. Liboureau: original concept, experimental design and work, data analysis, drafting and editing manuscript; G.A. Pearson: original concept, supervision and editing manuscript; E.A. Serrão: sampling and editing manuscript; N. Martins: original concept, experimental design, supervision and editing manuscript.

Additional information

Funding

This study received Portuguese national funds from FCT – Foundation for Science and Technology through SFRH/BPD/122567/2016 to NM (in transitional norm DL 57/2016/CP1361/CT0039, DOI 10.54499/DL57/2016/CP1361/CT0039), projects UIDB/04326/2020 (DOI:10.54499/UIDB/04326/2020), UIDP/04326/2020 (DOI:10.54499/UIDP/04326/2020) and LA/P/0101/2020 (DOI:10.54499/LA/P/0101/2020), and RESTORESEAS [EU-BiodivRestore-253 and FCT-DivRestore/0013/2020], MARAFRICA [AGA-KHAN/540316524/2019], and a Pew Marine Fellowship to EAS. Namibian sampling was funded by the [Benguela Current Convention] (BCC) project BCLME III, which received funds from the Global Environment Facility (GEF) and United Nations Development Programme (UNDP).