Sexual selection in seaweed? Testing Bateman's principles in the red alga Gracilaria gracilis

Abstract

In anisogamous species, sexual selection is expected to be stronger in males. Bateman's principles state that the variance in (i) reproductive and (ii) mating success is greater for males, and (iii) the relationship between reproductive success and mating success (the Bateman gradient) is also stronger for males than for females. Sexual selection, based on Bateman's principles, has been demonstrated in animals and some angiosperms, but never in a seaweed. Here we focus on the oogamous haploid-diploid rhodophyte Gracilaria gracilis in which previous studies have shown evidence for non-random mating, suggesting the existence of male-male competition and female choice. We estimated mating and reproductive success using paternity analyses in a natural population where up to 92% of fertilizations occurred between partners of that population. The results show that the variance in mating success is significantly greater in males than in females and that the Bateman gradient is positive only in males. Distance to female partners also explains a minor part of the variance in male mating success. Although there is no evidence for sexual dimorphism, our study supports the hypothesis that sexual selection occurs in G. gracilis, probably on male traits, even if we cannot observe, characterize or quantify them yet.

Keywords: Bateman gradient; dioicous species; haploid diploid life cycle; mating and reproductive success; paternity analyses; sessile marine organisms.

Figure 1.

Life cycle of Gracilaria gracilis. The individuals are fixed to the rocky substrate via a perennial holdfast. The deciduous erect thalli decay after reproduction in late autumn and grow back from the holdfast in spring. Diploid tetrasporophytes produce haploid spores from meiosis that develop into dioicous male and female haploid gametophytes. Spermatia (non-flagellated male gametes) are released into the water column. After fertilization, the zygote is retained on the female and develops into a complex, macroscopic post-fertilization structure: the cystocarp. One fertilization gives rise to thousands of identical diploid carpospores that, after release and germination, grow into new tetrasporophyte individuals.

Figure 2.

Map of the Cape Gris-Nez intertidal rock pool showing the locations of the 71 male (triangles) and the 70 female (circles) gametophyte individuals sampled within the population (the tetrasporophyte individuals are not shown). Mating success (i.e. the numbers of sexual partners) is proportional to filled symbol size. Females with missing information that were not included in Bateman analyses are indicated with open circles. The rock pool edges are shown in grey. The polygons within the rock pool indicate the presence of rocks.

Figure 3.

Relationship between reproductive and mating success and their distribution in males (dark blue) and females (green). Distribution of reproductive success (a,d), mating success (b,e) and the Bateman gradient (c,f) for males and females, respectively. The significance of the Bateman gradient, estimated by the slope of the linear regression, is indicated on the graph (c,f).

Figure 4.

Relationship between mating success and mean distance to partners (a) in males and (b) in females. The significance of the relationship, estimated by the slope of the linear regression, is shown on each graph.