Investigating biodiversity patterns across scales in freshwater mussels.

Hypotheses relating genomic diversity to community attributes such as abundance and species diversity attract attention from a wide and varied audience because their applications are twofold. First, testing such hypotheses can further a theoretical-and hopefully generalizable-understanding of the forces that assemble communities and create observed patterns of biodiversity. Second, relationships that hold true could ease the burden of data collection for conservation or other urgent applications; for example, a strong correlation between species diversity and genetic diversity could make it possible to use one as a proxy for the other, and focus limited resources on measuring the easier of the two without sacrificing information gained. In a From the Cover article in this issue of Molecular Ecology, Bucholz et al. (2023) explore the relationships between within-species genomic diversity, community relative abundance and community species richness, testing three types of ecological hypotheses in the freshwater mussel communities of the southeastern United States. They find positive relationships between mussel density and species richness, and between genomic diversity within a species and density of that species, but no robust support for the expectation of correlated genomic and species diversity. Their analyses highlight the among-species variability in relationships among these different levels of organization and also the complex ways in which interactions with the broader ecosystem (i.e. unionid mussels require fish hosts for maturation) affect these quantitative relationships, nonetheless pushing forward into the important frontier of community-wide genomic assessment for theoretical and conservation applications.

Extended phenotypes on coral reefs: cryptic phenotypes modulate coral-vermetid interactions.

Phenotypic variation can lead to variation in the strength and outcome of species interactions. Variation in phenotypic traits can arise due to plastic responses to environmental stimuli, underlying genetic variation, or both, and may reflect differences in the focal organism or aspects of the extended phenotype (e.g., associated microbes). We used a reciprocal transplant experiment of Porites corals to evaluate the role of plasticity vs. heritable diversity on phenotypic traits and performance of corals that varied in their prior exposure to vermetid gastropods, an organism known to reduce coral growth and survival. We measured a suite of phenotypic traits associated with coral performance, many of which showed a plastic response to vermetid exposure. Vermetids decreased calcification of corals, increased microbial diversity, and shifted microbial composition. Most traits also showed a signature of previous exposure environment that persisted even when exposure was reversed: i.e., under the same conditions, corals naïve to vermetids had slower calcification rates, thicker tissues, higher Symbiodiniaceae densities, and different microbiomes than corals previously exposed to vermetids. We suggest the phenotypic differences are heritable, as reefs with and without vermetids were comprised of two different mitotypes, that revealed high, consistent genetic variation. Vermetids were only found on the fast-growing coral mitotype that was characterized by thin tissue, and that likely had a history of disturbance. As extended phenotypes can have community impacts, we suggest vermetid, in addition to microbes, are part of the extended community phenotype of these corals. Coral genotypes can establish different reef trajectories, with thin-tissue types more prone to disturbance and subsequent colonization by other species, like vermetids, which can further facilitate the degradation of coral reefs. The effects of the extended phenotype of species likely influence heterogeneity across landscapes as well as temporal differences in community composition.

Examining an outlier: molecular diversity in the cirripedia.

Despite the typical assumption in studies of mitochondrial diversity that such data are useful for approximating population size and demography, studies of sequence diversity in mitochondrial DNA across the Metazoa have shown a surprising excess of rare alleles, a pattern associated either with strong selection or population growth. Previous work has shown that this bias toward an excess of rare alleles is typical across the Crustacea, and in particular, in the Cirripedia (barnacles). Here, we directly evaluate sequence data from studies of barnacle populations to ensure that inclusion of cryptic species is not the cause of this pattern. The results shown here reinforce previous studies that suggest caution in interpreting such patterns of allele frequencies, as they are likely to be influenced both by demographic changes and selection.

Overdominant maintenance of diversity in the sea star Pisaster ochraceus.

When individuals have higher evolutionary fitness because of being heterozygous at a given gene region, it is known as overdominance. Although overdominant selection could represent an important mechanism for maintaining genetic variation within species, the prevalence of this mode of selection appears to be relatively low. Identification of cases of true single-locus heterozygote advantage are thus useful reference points in our overall understanding of how various forms of balancing selection influence and maintain genetic variation in natural populations. Here we report the apparent long-term maintenance of diversity via overdominant selection with homozygous lethality at an elongation factor locus in the sea star Pisaster ochraceus. Observing this pattern in a gene with such major effects on protein assembly indicates that overdominant selection could be a more prevalent factor in maintaining allelic diversity in the wild than previously recognized.

Evolutionary dynamics of transferrin in Notropis.

This study reports on the development of comparative data for the transferrin (TF) gene in cyprinid fishes, focusing on the genus Notropis. While previous studies have suggested varied patterns of adaptation influencing the diversity at this gene locus both within and among species, sequence data for (TF) in Notropis exhibit limited evidence for selection. However, there are significant effects of sequence variation associated with Notropis lutipinnis, suggesting some form of diversifying selection acting among populations of this species. Overall, the gene performs well as a second locus for phylogenetic and biogeographic inference and may help improve description of the pattern and the process of diversification in Notropis.

Color polymorphism and genetic structure in the sea star Pisaster ochraceus.

The sea star Pisaster ochraceus is one of the more striking species on the rocky shores of the Northeast Pacific, in part due to the dramatic color polymorphism of the adults. Along the open Pacific coast, Pisaster populations are 6%-28% orange, with a small percentage of brilliant purple stars and a large percentage of reddish-brown to dull purple ones. However, populations in the San Juan Island Archipelago (Washington, USA) and the southern Strait of Georgia (British Columbia, Canada) are almost entirely brilliant purple. The factors that maintain the color polymorphism, and those that contribute to among-site variation in color frequencies, remain unknown. We examined the relationships between color frequencies and several ecological and morphological variables, and conducted a large-scale phylogeographic survey of Pisaster populations. We found very low population genetic structure, suggesting that gene flow is high and geographic variation in color frequencies is not a vestige of Pleistocene glacial refugia. Color frequencies are also unrelated to adult size and to the frequency of injury within a population. However, there are suggestive relationships between color frequency and diet, and with areas of potentially low salinity. We propose that, although the color polymorphism may have an underlying genetic component, the regional-scale variation in color frequency is ecologically controlled.

Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus.

Microbes and other organisms smaller than one to a few millimeters in size are hypothesized to have global populations, in contrast to the geographically restricted ranges of larger organisms. However, fungi, which routinely have reproductive propagules no larger than 10 micrometers, challenge the generality of this hypothesis because recent studies have shown that globally distributed morphological species embrace two or more geographically restricted phylogenetic species. We used the concordance of gene genealogies to recognize phylogenetic species in the globally distributed opportunistic human pathogenic fungus, Aspergillus fumigatus. Based on DNA sequence data of five loci for each of 63 individuals collected from five continents, we have delineated two phylogenetic species in this single morphological species. Unlike all other fungi examined to date, both genetically isolated groups showed a global distribution with no evidence of a correlation between genotype and geographic location. Sexual reproduction has never been observed in A. fumigatus, but when the same data were used to explore the association of alleles at the five loci for one of the phylogenetic species, evidence was found to support recombination. The discovery of a cryptic species is medically relevant because different species are likely to differ in virulence or drug resistance. The discovery of a globally distributed A. fumigatus species clade highlights the need for ecological studies of the fungus to either document global dispersal or propose alternative mechanisms by which it persists as single, global phylogenetic population.

Community genetics in the Northwestern Atlantic intertidal.

Our ability to make inferences about the processes acting upon a biological system can be dramatically improved through integration of information from other fields. In particular, this is true of the field of phylogeography, a discipline that attempts to describe geographical variation in species using neutral genetic diversity as a correlate of time. Through comparisons of information from multiple species, as well as background information about the abiotic environment and how it has changed over time, we should be able to reassemble many of the forces that were important in assembling the communities and community interactions found in a given region. Here I review the information available for coastal species in the northwestern Atlantic, and argue that an integration of ecological, genetic, geological and oceanographic information can illustrate emergent patterns of community genetics.

Biogeography of Asterias: North Atlantic climate change and speciation.

Fossil evidence suggests that the seastar genus Asterias arrived in the North Atlantic during the trans-Arctic interchange around 3.5 Ma. Previous genetic and morphological studies of the two species found in the Atlantic today suggested two possible scenarios for the speciation of A. rubens and A. forbesi. Through phylogenetic and population genetic analysis of data from a portion of the cytochrome oxidase I mitochondrial gene and a fragment of the ribosomal internal transcribed spacer region, I show that the formation of the Labrador Current 3.0 Ma was probably responsible for the initial vicariance of North Atlantic Asterias populations. Subsequent adaptive evolution in A. forbesi was then possible in isolation from the European species A. rubens. The contact zone between these two species formed recently, possibly due to a Holocene founding event of A. rubens in New England and the Canadian Maritimes.

A comparative study of asymmetric migration events across a marine biogeographic boundary.

In many nonclonal, benthic marine species, geographic distribution is mediated by the dispersal of their larvae. The dispersal and recruitment of marine larvae may be limited by temperature gradients that can affect mortality or by ocean currents that can directly affect the movements of pelagic larvae. We focus on Point Conception, a well-known biogeographic boundary between the Californian and Oregonian biogeographic provinces, to investigate whether ocean currents affect patterns of gene flow in intertidal marine invertebrates. The predominance of pelagically dispersing species with northern range limits at Point Conception suggests that ocean currents can affect species distributions by erecting barriers to the dispersal of planktonic larvae. In this paper, we investigate whether the predominantly southward currents have left a recognizable genetic signature in species with pelagically dispersing larvae whose ranges span Point Conception. We use patterns of genetic diversity and a new method for inferring cladistic migration events to test the hypothesis that southward currents increase southward gene flow for species with pelagically dispersing larvae. We collected mitochondrial DNA (mtDNA) sequence data for the barnacles Balanus glandula and Chthamalus fissus and also reanalyzed a previously published mtDNA dataset (Strongylocentrotus purpuratus, Edmands et al. 1996). For all three species, our cladistic approach identified an excess of southward migration events across Point Conception. In data from a fourth species with nondispersing larvae (Nucella emarginata, Marko 1998), our method suggests that ocean currents have not played a role in generating genetic structure.

Patterns of speciation inferred from mitochondrial DNA in North American Chthamalus (Cirripedia: Balanomorpha: Chthamaloidea).

Chthamalus is a cosmopolitan genus of high intertidal barnacles that are difficult to distinguish morphologically. This study focuses on a single subgeneric group of Chthamalus that is found on the coasts of North and Central America to determine the age and pattern of speciation among these species. Two comparisons of genetic divergence are made across the Panamanian Isthmus, allowing estimates of the substitution rate to be made for two mitochondrial genes coding for COI and 16S rRNA in these barnacles. These data suggest that the little morphological diversification that there has been in Chthamalus occurred early in the history of the genus, and subsequent radiations were probably induced by transient periods of population separation during late Miocene to Recent climatic changes.

Phylogeography and historical ecology of the North Atlantic intertidal.

Recent glaciation covered the full extent of rocky intertidal habitat along the coasts of New England and the Canadian Maritimes. To test whether this glaciation in fact caused wholesale extinction of obligate rocky intertidal invertebrates, and thus required a recolonization from Europe, we compared American and European populations using allelic diversity and techniques adapted from coalescent theory. Mitochondrial DNA sequences were collected from amphi-Atlantic populations of three cold-temperate obligate rocky intertidal species (a barnacle, Semibalanus balanoides, and two gastropods, Nucella lapillus and Littorina obtusata) and three cold-temperate habitat generalist species (a seastar, Asterias rubens; a mussel, Mytilus edulis, and an isopod, Idotea balthica). For many of these species we were able to estimate the lineage-specific mutation rate based on trans-Arctic divergences between Pacific and Atlantic taxa. These data indicate that some obligate rocky intertidal taxa have colonized New England from European populations. However, the patterns of persistence in North America indicate that other life-history traits, including mech anisms of dispersal, may be more important for surviving dramatic environmental and climatic change.