Footprints on water: The genetic wake of dispersal among reefs

Analysis of genetic data can reveal past and ongoing demographic connections between reef populations. The history, extent, and geography of isolation and exchange help to determine which populations are evolutionarily distinct and how to manage threatened reefs. Here the genetic approaches undertaken to understand connectivity among reefs are reviewed, ranging from early allozyme studies on genetic subdivision, through the use of sequence data to infer population histories, to emerging analyses that pull the influences of the past connections away from the effects of ongoing dispersal. Critically, some of these new approaches can infer migration and isolation over recent generations, thus offering the opportunity to answer many questions about reef connectivity and to better collaborate with ecologists and oceanographers to address problems that remain. © 2007 Springer-Verlag

No variation and low synonymous substitution rates in coral mtDNA despite high nuclear variation

BACKGROUND: The mitochondrial DNA (mtDNA) of most animals evolves more rapidly than nuclear DNA, and often shows higher levels of intraspecific polymorphism and population subdivision. The mtDNA of anthozoans (corals, sea fans, and their kin), by contrast, appears to evolve slowly. Slow mtDNA evolution has been reported for several anthozoans, however this slow pace has been difficult to put in phylogenetic context without parallel surveys of nuclear variation or calibrated rates of synonymous substitution that could permit quantitative rate comparisons across taxa. Here, I survey variation in the coding region of a mitochondrial gene from a coral species (Balanophyllia elegans) known to possess high levels of nuclear gene variation, and estimate synonymous rates of mtDNA substitution by comparison to another coral (Tubastrea coccinea). RESULTS: The mtDNA surveyed (630 bp of cytochrome oxidase subunit I) was invariant among individuals sampled from 18 populations spanning 3000 km of the range of B. elegans, despite high levels of variation and population subdivision for allozymes over these same populations. The synonymous substitution rate between B. elegans and T. coccinea (0.05%/site/10(6 )years) is similar to that in most plants, but 50–100 times lower than rates typical for most animals. In addition, while substitutions to mtDNA in most animals exhibit a strong bias toward transitions, mtDNA from these corals does not. CONCLUSION: Slow rates of mitochondrial nucleotide substitution result in low levels of intraspecific mtDNA variation in corals, even when nuclear loci vary. Slow mtDNA evolution appears to be the basal condition among eukaryotes. mtDNA substitution rates switch from slow to fast abruptly and unidirectionally. This switch may stem from the loss of just one or a few mitochondrion-specific DNA repair or replication genes

Sympatric sea shells along the sea\u27s shore: The geography of speciation in the marine gastropod Tegula

Uncertainty and controversy surround the geographical and ecological circumstances that create genetic differences between populations that eventually lead to reproductive isolation. Two aspects of marine organisms further complicate this situation: (1) many species possess planktonic larvae capable of great dispersal; and (2) obvious barriers to movement between populations are rare. Past studies of speciation in the sea have focussed on identifying the effects of past land barriers and on biogeographical breakpoints. However, assessing the role such undeniable barriers actually play in the initial divergence leading to reproductive isolation requires phylogenetic studies of recent radiations living in varying degrees of sympatry and allopatry to see which barriers (if any) tend to separate sister species. Here I refer phylogenetic relationship between 23 species of the marine snail Tegula using DNA sequences from two regions of the mitochondrial genome: cytochrome c oxidase I (COI) and the small ribosomal subunit (12S). These snails possess planktonic larvae with moderate dispersal capabilities and have speciated rapidly, with over 40 extant species arising since the genus first appeared in the mid-Miocene (about 15 M.Y.B.P.). Trees constructed from the COI and 12S regions (which yielded 205 and 137 phylogenetically informative sites, respectively)were robust with respect to tree-braiding method, bootstrapping, and the relative weightings of transitions, transversions, and gaps. Within clades where all extant species have been sampled, five of six identified sister species pairs broadly coexist on the same side of biogeographical boundaries. These data suggest strong geographical barriers to gene flow may not always be required for speciation m the sea; transient allopatry or even ecological barriers may suffice. A survey of the geographic distributions of marine radiations suggests that coastal distributions may favor the sympatry of sister taxa more than island distributions do

Long prereproductive selection and divergence by depth in a caribbean candelabrum coral

Long-lived corals, the foundation of modern reefs, often follow ecological gradients, so that populations or sister species segregate by habitat. Adaptive divergence maintains sympatric congeners after secondary contact or may even generate species by natural selection in the face of gene flow. Such ecological divergence, initially between alternative phenotypes within populations, may be aided by immigrant inviability, especially when a long period separates larval dispersal and the onset of reproduction, during which selection can sort lineages to match different habitats. Here, we evaluate the strength of one ecological factor (depth) to isolate populations by comparing the genes and morphologies of pairs of depth-segregated populations of the candelabrum coral Eunicea flexuosa across the Caribbean. Eunicea is endemic to the Caribbean and all sister species co-occur. Eunicea flexuosa is widespread both geographically and across reef habitats. Our genetic analysis revealed two depth-segregated lineages. Field survivorship data, combined with estimates of selection coefficients based on transplant experiments, suggest that selection is strong enough to segregate these two lineages. Genetic exchange between the Shallow and Deep lineages occurred either immediately after divergence or the two have diverged with gene flow. Migration occurs asymmetrically from the Shallow to Deep lineage. Limited recruitment to reproductive age, even under weak annual selection advantage, is sufficient to generate habitat segregation because of the cumulative prolonged prereproductive selection. Ecological factors associated with depth can act as filters generating strong barriers to gene flow, altering morphologies, and contributing to the potential for speciation in the sea

Marine radiations at small geographic scales: Speciation in neotropical reef gobies (Elacatinus)

Studies of speciation in the marine environment have historically compared broad-scale distributions and estimated larval dispersal potential to infer the geographic barriers responsible for allopatric speciation. However, many marine clades show high species diversity in geographically restricted areas where barriers are not obvious and estimated dispersal potential should bring many sister taxa into contact. Genetic differentiation at small (separation \u3c1000 \u3ekm) spatial scales could facilitate speciation by mechanisms other than the gradual accumulation of reproductive isolation during extended allopatry, such as ecological adaptation to local environmental conditions or the rapid evolution of genes tied to mate recognition, but the role of each of these possibilities has not been simultaneously explored for any species-rich marine tax on. Here, we develop a robust phylogenetic framework for 31 taxa from a species-rich group of Neotropical reef fishes (Gobiidae: Elacatinus) using 3230 bp from one mitochondrial and two nuclear gene regions. We use this framework to explore the contribution of large- and small-scale geographic isolation, ecological differentiation, and coloration toward the formation and maintenance of species. Although species of Elacatinus occur on both sides of the Isthmus of Panama, no sister species are separated by this barrier. Instead, our results indicate that sister taxa occur within oceans. Sister taxa usually differ by coloration, and more distantly related sympatric species frequently differ by resource use. This suggests that some combination of coloration and ecological differences may facilitate assortative mating at range boundaries or in sympatry. Overall, speciation in Elacatinus is consistent with a model of recurring adaptive radiations in stages taking place at small geographic scales. © 2005 The Society for the Study of Evolution. All rights reserved

Discordant coral–symbiont structuring: factors shaping geographical variation of Symbiodinium communities in a facultative zooxanthellate coral genus, Oculina

© 2016, Springer-Verlag Berlin Heidelberg. Understanding the factors that help shape the association between corals and their algal symbionts, zooxanthellae (Symbiodinium), is necessary to better understand the functional diversity and acclimatization potential of the coral host. However, most studies focus on tropical zooxanthellate corals and their obligate algal symbionts, thus limiting our full comprehension of coral–algal symbiont associations. Here, we examine algal associations in a facultative zooxanthellate coral. We survey the Symbiodinium communities associated with Oculina corals in the western North Atlantic and the Mediterranean using one clade-level marker (psbA coding region) and three fine-scale markers (cp23S–rDNA, b7sym15 flanking region, and b2sym17). We ask whether Oculina spp. harbor geographically different Symbiodinium communities across their geographic range and, if so, whether the host’s genetics or habitat differences are correlated with this geographical variation. We found that Oculina corals harbor different Symbiodinium communities across their geographical range. Of the habitat differences (including chlorophyll a concentration and depth), sea surface temperature is better correlated with this geographical variation than the host’s genetics, a pattern most evident in the Mediterranean. Our results suggest that although facultative zooxanthellate corals may be less dependent on their algal partners compared to obligate zooxanthellate corals, the Symbiodinium communities that they harbor may nevertheless reflect acclimatization to environmental variation among habitats

Comparative phylogeography in a genus of coral reef fishes: Biogeographic and genetic concordance in the Caribbean

Geographic barriers that limit the movement of individuals between populations may create or maintain phylogenetically discrete lineages. Such barriers are often inferred from geographic surveys of a single mitochondrial marker to identify phylogenetic splits. Mitochondrial DNA, however, has an effective population size one-fourth that of nuclear DNA, which can facilitate the rapid evolution of monophyletic mtDNA lineages in the absence of geographic barriers. The identification of geographic barriers will thus be more robust if barriers are proposed a priori, and tested with multiple independent genetic markers in multiple species. Here, we tested two proposed marine biogeographic breaks located at the Mona Passage in the Caribbean Sea and at the southern end of Exuma Sound in the Bahamas. We sequenced mitochondrial cytochrome b (400 bp) and nuclear rag1 (573 bp) for nine species and colour forms (183 individuals total) within the teleost genus Elacatinus (Gobiidae) that span the proposed breaks. Our results showed that Mona Passage separated mtcyb and rag1 lineages, with no genetic exchange between populations separated by just 23 km. However, the Central Bahamas barrier was only weakly supported by our data. Importantly, neither barrier coincided with deep genetic splits. This suggests that these two barriers did not initially isolate regional populations, but instead disrupt ongoing gene flow between regions. Our inferred relationships further suggested a division of the Caribbean region into northwestern and southeastern regions, a pattern reflected by some freshwater and terrestrial vertebrates. Our results, coupled with genetic and demographic data from other reef fishes and corals, provide robust support for the Mona Passage as a long-term biogeographic barrier for Caribbean animals. © 2006 Blackwell Publishing Ltd

Rapid evolution of fertilization selectivity and lysin cDNA sequences in Teguline gastropods

Proteins mediating intercellular recognition face opposing selective forces as they evolve: purifying selection to maintain function, and diversifying selection to alter specificity. Lysin is a 16-kDa protein which enables sperm of free-spawning marine snails to make a hole in the vitelline layer (VE) surrounding conspecific eggs. Previous work on abalone (Haliotis spp.) has shown that positive selection promotes rapid interspecific divergence of lysin. Here, we present data on the specificity of VE dissolution by four species of teguline gastropods, along with lysin cDNA sequences. The teguline and abalone lineages diverged over 250 MYA. As in abalone, VE dissolution by lysin in tegulines is species-selective, and positive selection promotes rapid interspecific divergence over the entire mature protein. Nonsynonymous substitution rates, calculated using a mtCOI molecular clock calibrated by two Tegula species separated by the Isthmus of Panama, are high (\u3e25 substitutions per site per 109 years). However, the extensive replacements in teguline lysins are overwhelmingly conservative with respect to type, charge, and polarity of residues. Predictions of secondary structure suggest that the size and position of α-helices are also conserved, even through pairwise amino acid identities between Haliotis rufescens and the different tegulines are less than 15%