Hope springs eternal in the starfish gonad: preserved potential for sexual reproduction in a single-clone population of a fissiparous starfish

Abstract

Among echinoderms, asexual reproduction by fission occurs in few species. This strategy is considered a temporary response to stressful conditions and usually alternates with sexual reproduction events; thus, monoclonal populations are extremely rare. The occurrence of a single-clone population of the starfish Coscinasterias tenuispina at Llançà (NW Mediterranean) allowed us to study intra-clonal variation of the reproductive cycle during a two-year study. The few developed gonads (all male) were found in winter months, coinciding with the minimum photoperiod (ρ = −0.82; P < 0.001) and lowest temperatures (ρ = −0.75; P < 0.001), only in best-fed individuals, indicating that food availability influences individual ability for gonad development. Fissiparity happened throughout all the sampled period, but its rate increased with warm temperatures (ρ = 0.68; P < 0.0001). In contrast to what has been reported in other species, no correlation between fission rates and population density was found. The population was maintained over time by asexual reproduction and remained monoclonal. Although sexual reproduction has probably not occurred in this all-male population for a long time, the ability to yearly produce mature gonads is retained by some individuals, indicating that potential to reproduce sexually may be preserved, even in the case of strictly asexual populations

Intraspecific genetic structure, divergence and high rates of clonality in an amphi‐Atlantic starfish

“…Sexual reproduction in the Canary Islands seems therefore to be more frequent than elsewhere in northeast Atlantic and Mediterranean Sea. This hypothesis is also supported by phenotypic information (Garcia‐Cisneros et al., ). Fission rates are inversely related to the starfish body size, being more frequent in smaller specimens (Emson & Wilkie, ) as those found in the Mediterranean Sea, and less frequent in larger specimens as those found in the Canary Islands (Garcia‐Cisneros et al., , ).…”

“…This hypothesis is also supported by phenotypic information (Garcia‐Cisneros et al., ). Fission rates are inversely related to the starfish body size, being more frequent in smaller specimens (Emson & Wilkie, ) as those found in the Mediterranean Sea, and less frequent in larger specimens as those found in the Canary Islands (Garcia‐Cisneros et al., , ). Hence, higher prevalence of sexual reproduction and the existence of planktonic larvae promoting gene flow explain the low genetic distances observed among Tazacorte, Abades and Lanzarote at the Canary Islands.…”

“…However, due to the small number of haplotypes found in C. tenuispina , related to the prevalence of asexual reproduction, exploring demographic expansions cannot be used as a straightforward approach to test the hypothesis of a recent Mediterranean colonization. Nevertheless, the equivalent amphi‐Atlantic distribution of A. lixula and C. tenuispina, similar sexual reproduction patterns (Garcia‐Cisneros et al., ; Wangensteen, Turon, Casso, & Palacín, ), and equivalent phylogeography with absence of a Mediterranean lineage (Wangensteen et al., ) may also suggest a recent colonization of C. tenuispina in the Mediterranean. Our results demonstrate that asexual reproduction is common in C. tenuispina , as observed by the presence of clones and significant excess of heterozygotes (Balloux et al., ; de Meeûs et al., ) in all populations. Nevertheless, there are large differences in clonality rates among populations and geographical areas, a general pattern observed in marine colonial invertebrates with asexual reproduction (e.g., Ayre & Hughes, ; Zilberberg et al., ).…”

“…The genetic homogeneity at the western Mediterranean should not be interpreted as current and extended gene flow between sites. All clones analysed across the western Mediterranean were identified as males (Garcia‐Cisneros et al., ; and author's unpublished data), and therefore, sexual reproduction along this geographical area seems unlikely. The presence of only one clone increases the effective population size almost to infinite, thereby reducing the loss of genetic diversity due to stochastic events, and the probability of genetic divergence among populations due to genetic drift in absence of gene flow (Balloux et al., ; Delmotte et al., ).…”

“…So high clonality in C. tenuispina may be explained by unfavourable conditions preventing maturation of the gonads and larva survival (Eckert, ) in some areas recently colonized. A two‐year monitoring of the biological cycle of C. tenuispina at the northwestern Mediterranean (Garcia‐Cisneros et al., ) demonstrated an annual pattern of gonad maturation and potential spawning during winter months when mean seawater temperature was around 13–16°C. This annual cycle is probably determined by genetic traits selected for adapting to the prevalent conditions in their original distribution areas, and recent colonizers would retain this genetic programme (Wangensteen et al., ), whereas splitting seems irregular across the year and likely influenced by environmental fluctuations (Garcia‐Cisneros et al., ).…”