Population genetics of reef coral endosymbionts (Symbiodinium, Dinophyceae)

Abstract

Symbiodinium is a diverse genus of unicellular dinoflagellate symbionts associating with various marine protists and invertebrates. Although the broadscale diversity and phylogenetics of the Symbiodinium complex is well established, there have been surprisingly few data on fine-scale population structure and biogeography of these dinoflagellates. Yet population-level processes contribute strongly to the biology of Symbiodinium, including how anthropogenic-driven global climate change impacts these symbionts and their host associations. Here, we present a synthesis of population-level characteristics for Symbiodinium, with an emphasis on how phylogenetic affinities, dynamics within and among host individuals, and a propensity towards clonality shape patterns on and across reefs. Major inferences include the following: (i) Symbiodinium populations within individual hosts are comprised mainly of cells belonging to a single or few genetic clones. (ii) Symbiont populations exhibit a mixed mode of reproduction, wherein at least one sexual recombination event occurs in the genealogy between most genotypes, but clonal propagation predominates overall. (iii) Mutualistic Symbiodinium do not perpetually persist outside their hosts, instead undergoing turnover and replacement via the continuous shedding of viable clonal cells from host individuals. (iv) Symbiont populations living in the same host, but on different reefs, are often genetically subdivided, suggesting low connectivity, adaptation to local conditions, or prolific asexual reproduction and low effective population sizes leading to disproportionate success within and among hosts. Overall, this synthesis forms a basis for future investigations of coral symbiosis ecology and evolution as well as delimitation of species boundaries in Symbiodinium and other eukaryotic microorganisms.

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

“…This fine‐scale spatial genetic structure is consistent with patterns observed with microsatellite markers for Cladocopium populations on the Great Barrier Reef (Howells, van Oppen, & Willis, ; Howells, Willis, Bay, & Oppen, ) and in the Caribbean (Thornhill et al, ). Thus, it is likely that Cladocopium populations in the Persian Gulf are also differentiated due to limited dispersal and recruitment among sites and predominant asexual reproduction within sites (Thornhill, Howells, Wham, Steury, & Santos, ). An alternative explanation is that site‐specific sequences and type profiles represent functionally distinct genotypes of Symbiodiniaceae that are adapted to local environmental conditions.…”

“…In purely clonal populations, each individual cell would be expected to comprise a mixture of intragenomic variants in equal proportions. However, infrequent recombination (Thornhill et al, ) and/or somatic mutations (van Oppen, Souter, Howells, Heyward, & Berkelmans, ) could result in unequal proportions of intragenomic variants across offspring generations (Wilkinson, Fisher, van Oppen, & Davy, ). For example, the co‐occurrence of C3 and C3gulf may represent recombination between distinct lineages, with functional differences among purebred, hybrid and backcross generations (Wilkinson et al, ).…”

Environmental latitudinal gradients and host‐specificity shape Symbiodiniaceae distribution in Red Sea Porites corals

“…Most recently, the SymPortal analytical framework (http://www.symportal.org/; https://github.com/didillysquat/SymPortal_framework; Hume et al, ) has been developed to make use of this intragenomic diversity for resolving genetic delineations using next‐generation sequencing (hereafter ‘NGS’) ITS2 data. By leveraging the informative nature of Symbiodiniaceae intragenomic diversity, finer scale resolutions of genetic delineations are now possible; these delineations far surpass what were previously achievable with the ITS2 marker (Hume et al, ; Smith et al, ; Thornhill, Howells, Wham, Steury, & Santos, ).…”

Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes

“…Although symbiont species such as S. psygmophilum can have a broad distribution at the species level (LaJeunesse et al 2012, dispersal of symbionts at the population level is generally thought to be limited (see review by Thornhill et al 2017). Moreover, observations between 1992 and 2010 suggest that northward expansion of O. patagonica has occurred through a small number of longdistance dispersal events (between 76 and 182 km; Serrano et al 2013), possibly limited by the oceanographic barrier represented by the Ibiza Channel ( Fig.…”