Higher reproductive success for chimeras than solitary individuals in the kelp Lessonia spicata but no benefit for individual genotypes

Abstract

Chimerism is a peculiar, yet widespread, type of group living in which genetically heterogeneous entities are created through fusion between conspecifics. Here we tested whether chimerism provides direct benefits to the kelp Lessonia spicata, by analyzing its consequences on reproductive investment and success, at both the genotype and thallus levels. In addition, we quantified the frequency of chimerism in two natural populations, tested if group members were close kin, and evaluated the effects of relatedness and the number of genotypes per thallus on reproduction. Chimeric thalli were frequent ([60 %) in natural populations of L. spicata. In most cases, average intragroup relatedness was not significantly different from the background population. Reproductive investment was not significantly affected by the type of thallus (chimeric versus non-chimeric), by the number of genotypes per thallus or the average relatedness within thallus. Chimerism did not result in net benefits or costs in terms of genotypic reproductive success or probability of reproducing at the genotypic level. Yet, at the thallus level, chimerism increased reproductive success and the probability of reproducing, since more than one genotype reproduced in chimeric thallus. At the population level, chimerism affects L. spicata reproductive success by allowing the coexistence of a higher density of potential reproducers and mates compared to a scenario with only non-chimeric thallus. Chimerism may then have an important effect on the effective population size and possibly in reducing selfing rates.

Frequency of chimerism in populations of the kelp Lessonia spicata in central Chile

“…Regardless of the genetic approaches used, the highest harvested population, Pichicuy showed that 26.7–86.7% of plants were chimeric, followed by Maitencillo (53.3–66.7%) and La Puntilla (6.7–33%). Most of these frequency values fall within the range of values found in the only other study on chimerism frequency for natural populations of this species in Chile Lessonia spicata (60–90%, [ 31 ]). However, in that study [ 31 ] kelp holdfasts were not considered and the occurrence of methodological errors (electrophoresis artifacts) were not evaluated.…”

“…Most of these frequency values fall within the range of values found in the only other study on chimerism frequency for natural populations of this species in Chile Lessonia spicata (60–90%, [ 31 ]). However, in that study [ 31 ] kelp holdfasts were not considered and the occurrence of methodological errors (electrophoresis artifacts) were not evaluated. In our study we found that stipes were genetically homogenous without mixing tissues from base to lamina.…”

“…spicata (63–87%, [ 26 ]). Similarly, a recent study in two National Reserves (Pingüino de Humbold and Fray Jorge, [ 31 ]) evidenced a high frequency (>60%) of L . spicata plants composed by two or more genetically heterogeneous stipes, but none of these showed mixed tissues in the same stipe.…”

Coral chimerism as an evolutionary rescue mechanism to mitigate global climate change impacts

“…Coral chimerism is associated with the trait of gregarious settlement (Amar et al, 2008;Barki et al, 2002;Boschma, 1929;Duerden, 1902;Frank et al, 1997;Jiang et al, 2015;Linden & Rinkevich, 2017;Mizrahi et al, 2014 revealing that fusion has clear benefits for survival, and/or growth, at early ontogenic and astogenic phases (Amar et al, 2008;Mizrahi et al, 2014;Raymundo & Maypa, 2004). The immediate increase in body size following the formation of a chimera has an important bearing on a wide range of biological and ecological traits, including enhanced reproductive success (Casares & Faugeron, 2016), eased onset of reproduction, improved competitive capabilities along vulnerable juvenile stages, reduced whole-entity mortality rates (Buss, 1982) as well as protection from adverse environmental conditions (McIntire & Fajardo, 2011;Wernberg, 2005). Another phenomenon is the enhanced preferential gregarious settlement of coral planulae on injured/broken coral branches, which further facilitates the healing of damaged corals.…”

Invasiveness, chimerism and genetic diversity

“…In tunicates, multipartner chimeras developed into vital and stable entities with potentially higher fitness, due to exhibiting different phenotypic combinations in adverse environmental conditions (Rinkevich, ; Rinkevich & Yankelevich, ). Likewise, the chimeric red algae Mazzaella laminarioides (Rhodophyta) demonstrated better tolerance to environmental stressors and enhanced phenotypic plasticity (Medina et al., ); chimeras of the kelp Lessonia spicata show higher reproductive success (Araujo Casares & Faugeron, ) and the marine angiosperm Zostera marina , a wide‐ranging species in the Northern Hemisphere, indicated higher levels of chimerism in populations residing in both the northern and southern boundaries of their distribution in Europe (Reusch & Bostrom, ). Nonetheless, while these hypothetical ideas seem promising, the experimental data are limited and inconclusive.…”