The consequences of partial clonality on the spatiotemporal genetic structure of the red alga Chondria tumulosa (Ceramiales, Rhodophyta)

Abstract

The relative rates of sexual versus clonal reproduction partition genetic diversity, but the quantification of these rates remains limited in natural populations. This knowledge gap is particularly acute among tropical macroalgae. Chondria tumulosa is a red macroalga that has been documented at high abundance in the three northernmost atolls in the Papahānaumokuākea Marine National Monument. We sampled thalli at Manawai (2021, 2023), at Kuaihelani (2022, 2023), and at Hōlanikū (2023) to characterize the reproductive mode and patterns of gene flow. Tetrasporophytes overwhelmingly dominated, although eight cystocarpic female gametophytes (<1%) were documented. We observed evidence of very high clonal rates, accompanied by an increase in homozygosity. Surprisingly, our temporal analyses suggested site-specific trends in the predominance of selfing, outcrossing, or clonality. A very small haploid proportion combined with high genetic drift rendered temporal analyses of genotypic frequencies challenging to implement and interpret, such that point estimates were a better reflection of reproductive mode variation. Genetic differentiation increased with geographic distance, with strong temporal and spatial structure. The reduced genetic diversity, decreasing heterozygosity over time, and high spatial and temporal genetic discontinuities combined with the dominance of tetrasporophytes suggest a recent introduction of C. tumulosa in this region, possibly via marine debris rather than a regional opportunistic species undergoing population eruptions. Future studies should focus on identifying the native range to document the ecological and evolutionary shifts that have facilitated the rapid increase and spread of C. tumulosa and its potential similarities to other invasive haploid-diploid algae.