Cophylogeny and specificity between cryptic coral species (Pocillopora spp.) at Mo′orea and their symbionts (Symbiodiniaceae)

Abstract

The congruence between phylogenies of tightly associated groups of organisms (cophylogeny) reflects evolutionary links between ecologically important interactions. However, despite being a classic example of an obligate symbiosis, tests of cophylogeny between scleractinian corals and their photosynthetic algal symbionts have been hampered in the past because both corals and algae contain genetically unresolved and morphologically cryptic species. Here, we studied co‐occurring, cryptic Pocillopora species from Mo′orea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the host Pocillopora (using complete mitochondrial genomes, genomic loci, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbAncr markers) and tested for cophylogeny. The analysis supported the presence of five Pocillopora species on the fore reef at Mo′orea that mostly hosted either Cladocopium latusorum or C. pacificum. Only Pocillopora species hosting C. latusorum also hosted taxa from Symbiodinium and Durusdinium. In general, the Cladocopium phylogeny mirrored the Pocillopora phylogeny. Within Cladocopium species, lineages also differed in their associations with Pocillopora haplotypes, except those showing evidence of nuclear introgression, and with depth in the two most common Pocillopora species. We also found evidence for a new Pocillopora species (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of these Pocillopora and Cladocopium species and lineages suggest that symbiont speciation is driven by niche diversification in the host, but there is still evidence for symbiont flexibility in some cases.

Branching coral morphology affects physiological performance in the absence of colony integration

“…represent an assemblage of cryptic species with differential bleaching susceptibility [ 35 ]. In Pocillopora spp., we have shown that morphological taxonomy [ 36 ] is a poor indicator of species identity [ 35 , 37 ], and therefore, it is possible that both of our trials contained more than one species. Since at least some of the species in this complex are physiologically unequal as demonstrated by contrasting bleaching susceptibility [ 35 ], it is also possible that they differentially translate colony integration into emergent aspects of colony performance.…”

“…Trials were conducted in 150 l tanks that were heated, mixed, chilled, illuminated and supplied with CO 2 gas. We targeted P. verrucosa for collection based on morphology [ 36 ], although we probably worked with cryptic species [ 35 , 37 ] and, hereafter, we refer to our study organism as Pocillopora spp. Sampled corals were used to prepare single branches (nubbins), ‘artificial colonies’ (aggregates) of nubbins from the same genotype that are glued to a plastic base in an array creating the branch spacing of natural colonies (but lacking integration because the nubbins are not connected by tissue or skeleton) and intact colonies (colonies).…”

Disparate population and holobiont structure of pocilloporid corals across the Red Sea gradient demonstrate species‐specific evolutionary trajectories

“…Notably, P. verrucosa typically hosts Cladocopium sp. across the Pacific Ocean at large, not Symbiodinium , which may provide further evidence to the argument that Pocillopora ‐ Symbiodinium associations represent an adaptation to warmer and nutrient‐rich waters (Johnston et al, 2022; Turnham et al, 2021). Although the Red Sea P. verrucosa Cladocopium C1 has been portrayed as a high‐performance microalgal partner (Sawall et al, 2014, 2015), its association might be constrained to narrow environmental regimes.…”

Environmental and geographical factors structure cauliflower coral's algal symbioses across the Indo‐Pacific

“…However, there remains a knowledge gap concerning where and why particular Symbiodiniaceae taxa are associated with particular coral genera. To date, coral studies have typically focused on the factors structuring these symbioses in either a single geographical location (Johnston, Cunning, & Burgess, 2022;O'Brien et al, 2020;Osman et al, 2020;Pollock et al, 2018;Ricci et al, 2022) or for a single Symbiodiniaceae genus at the regional level (Turnham et al, 2021).…”

“…However, there remains a knowledge gap concerning where and why particular Symbiodiniaceae taxa are associated with particular coral genera. To date, coral studies have typically focused on the factors structuring these symbioses in either a single geographical location (Johnston, Cunning, & Burgess, 2022; O'Brien et al, 2020; Osman et al, 2020; Pollock et al, 2018; Ricci et al, 2022) or for a single Symbiodiniaceae genus at the regional level (Turnham et al, 2021). It is important to consider how environmental and geographical factors together are driving the establishment and maintenance of this symbiotic relationship, as the diversity, distribution and stability of Symbiodiniaceae communities is central to coral's future in an increasingly warmer, high CO 2 world.…”