Defining and quantifying the core microbiome: Challenges and prospects.

The term "core microbiome" has become widely used in microbial ecology over the last decade. Broadly, the core microbiome refers to any set of microbial taxa, or the genomic and functional attributes associated with those taxa, that are characteristic of a host or environment of interest. Most commonly, core microbiomes are measured as the microbial taxa shared among two or more samples from a particular host or environment. Despite the popularity of this term and its growing use, there is little consensus about how a core microbiome should be quantified in practice. Here, we present a brief history of the core microbiome concept and use a representative sample of the literature to review the different metrics commonly used for quantifying the core. Empirical analyses have used a wide range of metrics for quantifying the core microbiome, including arbitrary occurrence and abundance cutoff values, with the focal taxonomic level of the core ranging from phyla to amplicon sequence variants. However, many of these metrics are susceptible to sampling and other biases. Developing a standardized set of metrics for quantifying the core that accounts for such biases is necessary for testing specific hypotheses about the functional and ecological roles of core microbiomes.

Shell mineralogy of a foundational marine species, Mytilus californianus, over half a century in a changing ocean.

Anthropogenic warming and ocean acidification are predicted to negatively affect marine calcifiers. While negative effects of these stressors on physiology and shell calcification have been documented in many species, their effects on shell mineralogical composition remains poorly known, especially over longer time periods. Here, we quantify changes in the shell mineralogy of a foundation species, Mytilus californianus, under 60 y of ocean warming and acidification. Using historical data as a baseline and a resampling of present-day populations, we document a substantial increase in shell calcite and decrease in aragonite. These results indicate that ocean pH and saturation state, not temperature or salinity, play a strong role in mediating the shell mineralogy of this species and reveal long-term changes in this trait under ocean acidification.

Decade-scale stability and change in a marine bivalve microbiome.

Predicting how populations and communities of organisms will respond to anthropogenic change is of paramount concern in ecology today. For communities of microorganisms, however, these predictions remain challenging, primarily due to data limitations. Information about long-term dynamics of host-associated microbial communities, in particular, is lacking. In this study, we use well-preserved and freshly collected samples of soft tissue from a marine bivalve host, Donax gouldii, at a single site to quantify the diversity and composition of its microbiome over a decadal timescale. Site-level measurements of temperature, salinity and chlorophyll a allowed us to test how the microbiome of this species responded to two natural experiments: a seasonal increase in temperature and a phytoplankton bloom. Our results show that ethanol-preserved tissue can provide high-resolution information about temporal trends in compositions of host-associated microbial communities. Specifically, we found that the richness of amplicon sequence variants (ASVs) associated with D.gouldii did not change significantly over time despite increases in water temperature (+1.6°C due to seasonal change) and chlorophyll a concentration (more than ninefold). The phylogenetic composition of the communities, on the other hand, varied significantly between all collection years, with only six ASVs persisting over our sampling period. Overall, these results suggest that the diversity of microbial taxa associated with D.gouldii has remained stable over time and in response to seasonal environmental change over the course of more than a decade, but such stability is underlain by substantial turnover in the composition of the microbiome.

Fossils, phylogenies, and the challenge of preserving evolutionary history in the face of anthropogenic extinctions.

Anthropogenic impacts are endangering many long-lived species and lineages, possibly leading to a disproportionate loss of existing evolutionary history (EH) in the future. However, surprisingly little is known about the loss of EH during major extinctions in the geological past, and thus we do not know whether human impacts are pruning the tree of life in a manner that is unique in the history of life. A major impediment to comparing the loss of EH during past and current extinctions is the conceptual difference in how ages are estimated from paleontological data versus molecular phylogenies. In the former case the age of a taxon is its entire stratigraphic range, regardless of how many daughter taxa it may have produced; for the latter it is the time to the most recent common ancestor shared with another extant taxon. To explore this issue, we use simulations to understand how the loss of EH is manifested in the two data types. We also present empirical analyses of the marine bivalve clade Pectinidae (scallops) during a major Plio-Pleistocene extinction in California that involved a preferential loss of younger species. Overall, our results show that the conceptual difference in how ages are estimated from the stratigraphic record versus molecular phylogenies does not preclude comparisons of age selectivities of past and present extinctions. Such comparisons not only provide fundamental insights into the nature of the extinction process but should also help improve evolutionarily informed models of conservation prioritization.

Convergence, divergence, and parallelism in marine biodiversity trends: Integrating present-day and fossil data.

Paleontological data provide essential insights into the processes shaping the spatial distribution of present-day biodiversity. Here, we combine biogeographic data with the fossil record to investigate the roles of parallelism (similar diversities reached via changes from similar starting points), convergence (similar diversities reached from different starting points), and divergence in shaping the present-day latitudinal diversity gradients of marine bivalves along the two North American coasts. Although both faunas show the expected overall poleward decline in species richness, the trends differ between the coasts, and the discrepancies are not explained simply by present-day temperature differences. Instead, the fossil record indicates that both coasts have declined in overall diversity over the past 3 My, but the western Atlantic fauna suffered more severe Pliocene-Pleistocene extinction than did the eastern Pacific. Tropical western Atlantic diversity remains lower than the eastern Pacific, but warm temperate western Atlantic diversity recovered to exceed that of the temperate eastern Pacific, either through immigration or in situ origination. At the clade level, bivalve families shared by the two coasts followed a variety of paths toward today's diversities. The drivers of these lineage-level differences remain unclear, but species with broad geographic ranges during the Pliocene were more likely than geographically restricted species to persist in the temperate zone, suggesting that past differences in geographic range sizes among clades may underlie between-coast contrasts. More detailed comparative work on regional extinction intensities and selectivities, and subsequent recoveries (by in situ speciation or immigration), is needed to better understand present-day diversity patterns and model future changes.

Shaping the Latitudinal Diversity Gradient: New Perspectives from a Synthesis of Paleobiology and Biogeography.

An impediment to understanding the origin and dynamics of the latitudinal diversity gradient (LDG)-the most pervasive large-scale biotic pattern on Earth-has been the tendency to focus narrowly on a single causal factor when a more synthetic, integrative approach is needed. Using marine bivalves as a model system and drawing on other systems where possible, we review paleobiologic and biogeographic support for two supposedly opposing views, that the LDG is shaped primarily by (a) local environmental factors that determine the number of species and higher taxa at a given latitude (in situ hypotheses) or (b) the entry of lineages arising elsewhere into a focal region (spatial dynamics hypotheses). Support for in situ hypotheses includes the fit of present-day diversity trends in many clades to such environmental factors as temperature and the correlation of extinction intensities in Pliocene bivalve faunas with net regional temperature changes. Support for spatial dynamics hypotheses includes the age-frequency distribution of bivalve genera across latitudes, which is consistent with an out-of-the-tropics dynamic, as are the higher species diversities in temperate southeastern Australia and southeastern Japan than in the tropical Caribbean. Thus, both in situ and spatial dynamics processes must shape the bivalve LDG and are likely to operate in other groups as well. The relative strengths of the two processes may differ among groups showing similar LDGs, but dissecting their effects will require improved methods of integrating fossil data with molecular phylogenies. We highlight several potential research directions and argue that many of the most dramatic biotic patterns, past and present, are likely to have been generated by diverse, mutually reinforcing drivers.

Historical baselines and the future of shell calcification for a foundation species in a changing ocean.

Seawater pH and the availability of carbonate ions are decreasing due to anthropogenic carbon dioxide emissions, posing challenges for calcifying marine species. Marine mussels are of particular concern given their role as foundation species worldwide. Here, we document shell growth and calcification patterns in Mytilus californianus, the California mussel, over millennial and decadal scales. By comparing shell thickness across the largest modern shells, the largest mussels collected in the 1960s-1970s and shells from two Native American midden sites (∼1000-2420 years BP), we found that modern shells are thinner overall, thinner per age category and thinner per unit length. Thus, the largest individuals of this species are calcifying less now than in the past. Comparisons of shell thickness in smaller individuals over the past 10-40 years, however, do not show significant shell thinning. Given our sampling strategy, these results are unlikely to simply reflect within-site variability or preservation effects. Review of environmental and biotic drivers known to affect shell calcification suggests declining ocean pH as a likely explanation for the observed shell thinning. Further future decreases in shell thickness could have significant negative impacts on M. californianus survival and, in turn, negatively impact the species-rich complex that occupies mussel beds.

Out of the tropics, but how? Fossils, bridge species, and thermal ranges in the dynamics of the marine latitudinal diversity gradient.

Latitudinal diversity gradients are underlain by complex combinations of origination, extinction, and shifts in geographic distribution and therefore are best analyzed by integrating paleontological and neontological data. The fossil record of marine bivalves shows, in three successive late Cenozoic time slices, that most clades (operationally here, genera) tend to originate in the tropics and then expand out of the tropics (OTT) to higher latitudes while retaining their tropical presence. This OTT pattern is robust both to assumptions on the preservation potential of taxa and to taxonomic revisions of extant and fossil species. Range expansion of clades may occur via "bridge species," which violate climate-niche conservatism to bridge the tropical-temperate boundary in most OTT genera. Substantial time lags (∼5 Myr) between the origins of tropical clades and their entry into the temperate zone suggest that OTT events are rare on a per-clade basis. Clades with higher diversification rates within the tropics are the most likely to expand OTT and the most likely to produce multiple bridge species, suggesting that high speciation rates promote the OTT dynamic. Although expansion of thermal tolerances is key to the OTT dynamic, most latitudinally widespread species instead achieve their broad ranges by tracking widespread, spatially-uniform temperatures within the tropics (yielding, via the nonlinear relation between temperature and latitude, a pattern opposite to Rapoport's rule). This decoupling of range size and temperature tolerance may also explain the differing roles of species and clade ranges in buffering species from background and mass extinctions.

Global environmental predictors of benthic marine biogeographic structure.

Analyses of how environmental factors influence the biogeographic structure of biotas are essential for understanding the processes underlying global diversity patterns and for predicting large-scale biotic responses to global change. Here we show that the large-scale geographic structure of shallow-marine benthic faunas, defined by existing biogeographic schemes, can be predicted with 89-100% accuracy by a few readily available oceanographic variables; temperature alone can predict 53-99% of the present-day structure along coastlines. The same set of variables is also strongly correlated with spatial changes in species compositions of bivalves, a major component of the benthic marine biota, at the 1° grid-cell resolution. These analyses demonstrate the central role of coastal oceanography in structuring benthic marine biogeography and suggest that a few environmental variables may be sufficient to model the response of marine biogeographic structure to past and future changes in climate.

Selectivity of terrestrial gastropod extinctions on an oceanic archipelago and insights into the anthropogenic extinction process.

Anthropogenic impacts have led to widespread extinctions of species on oceanic islands but the nature of many of these extinctions remains poorly known. Here we investigate extinction selectivities of terrestrial gastropods from the Ogasawara archipelago in the northwest Pacific, where anthropogenic threats have changed over time, shifting primarily from the effects of habitat loss to predation by a variety of different predators. Across all of the islands, extinct species had significantly smaller geographic ranges compared with species that are still alive, but among the surviving species, ranges of those that are currently declining due to human impacts do not differ significantly from those that are not threatened. Extinctions were selective with respect to spire index (SI) of shells, a trait of potential functional importance, but the relationship between body size and extinction vulnerability varied among extinction agents, some of which were strongly size selective, whereas others were not. Overall, whereas anthropogenic impacts have resulted in nonrandom losses of phenotypic diversity, the patterns of selectivity are complex, vary among islands, and with the type of threat. As extinction agents have changed historically, so has the pattern of loss. Because of the changing nature of anthropogenic impacts, resiliency to one type of threat does not guarantee long-term survival of species and future patterns of biodiversity loss on these islands are likely to be different from those in the past.

Diversity, distribution and intrinsic extinction vulnerability of exploited marine bivalves.

Marine bivalves are important components of ecosystems and exploited by humans for food across the world, but the intrinsic vulnerability of exploited bivalve species to global changes is poorly known. Here, we expand the list of shallow-marine bivalves known to be exploited worldwide, with 720 exploited bivalve species added beyond the 81 in the United Nations FAO Production Database, and investigate their diversity, distribution and extinction vulnerability using a metric based on ecological traits and evolutionary history. The added species shift the richness hotspot of exploited species from the northeast Atlantic to the west Pacific, with 55% of bivalve families being exploited, concentrated mostly in two major clades but all major body plans. We find that exploited species tend to be larger in size, occur in shallower waters, and have larger geographic and thermal ranges-the last two traits are known to confer extinction-resistance in marine bivalves. However, exploited bivalve species in certain regions such as the tropical east Atlantic and the temperate northeast and southeast Pacific, are among those with high intrinsic vulnerability and are a large fraction of regional faunal diversity. Our results pinpoint regional faunas and specific taxa of likely concern for management and conservation.

Anthropogenic harvesting pressure and changes in life history: insights from a rocky intertidal limpet.

The importance of large breeding individuals for maintaining the health of marine fish and invertebrate populations has long been recognized. Unfortunately, decades of human harvesting that preferentially remove larger individuals have led to drastic reductions in body sizes of many of these species. Such size-selective harvesting is particularly worrisome for sequentially hermaphroditic species where the larger size classes are composed primarily of one sex. Whether these species can maintain stable sex ratios under sustained harvesting pressure depends on the level of plasticity of their life-history traits. Here, we show that populations of a marine limpet (Lottia gigantea) can adjust a fundamental aspect of their life history (the timing of sex change) when subjected to size-selective harvesting. As predicted by theoretical models, individuals from harvested populations change sex at smaller sizes and grow at slower rates compared to individuals from protected populations. In addition, the relative size at which the change from male to female occurs remains constant (~0.75; size at sex change/maximum size) across populations, regardless of harvesting pressure. Our results show that population-level demographic and life-history data, in conjunction with existing theory, can be sufficient to predict the responses of sequential hermaphrodites to harvesting pressure. Furthermore, they suggest such species can potentially adapt to size-selective harvesting.

A macroevolutionary perspective on species range limits.

Understanding the factors that determine the geographic range limits of species is important for many questions in ecology, evolution and conservation biology. These limits arise from complex interactions among ecology and dispersal ability of species and the physical environment, but many of the underlying traits can be conserved among related species and clades. Thus, the range limits of species are likely to be influenced by their macroevolutionary history. Using palaeontological and biogeographic data for marine bivalves, we find that the range limits of genera are significantly related to their constituent species richness, but the effects of age are weak and inconsistent. In addition, we find a significant phylogenetic signal in the range limits at both genus and family levels, although the strength of this effect shows interoceanic variation. This phylogenetic conservatism of range limits gives rise to an evolutionary pattern where wide-ranging lineages have clusters of species within the biogeographic provinces, with a few extending across major boundaries.

The use of sighting records to infer species extinctions: an evaluation of different methods.

In the absence of long-term monitoring data, inferences about extinctions of species and populations are generally based on past observations about the presence of a particular species at specified places and times (sightings). Several methods have been developed to estimate the probability and timing of extinctions from records of such sightings, but they differ in their computational complexity and assumptions about the nature of the sighting record. Here we use simulations to evaluate the performance of seven methods proposed to estimate the upper confidence limit on extinction times under different extinction and sampling scenarios. Our results show that the ability of existing methods to correctly estimate the timing of extinctions varies with the type of extinction (sudden vs. gradual) and the nature of sampling effort over time. When the probability of sampling a species declines over time, many of the methods perform poorly. On the other hand, the simulation results also suggest that as long as the choice of the method is determined by the nature of the underlying sighting data, existing methods should provide reliable inferences about the timing of past extinctions.

Diversity and composition of intertidal gastropod microbiomes across a major marine biogeographic boundary.

Marine biogeographic boundaries act as barriers to dispersal for many animal species, thereby creating distinctive faunas on either side. However, how such boundaries affect the distributions of microbial taxa remains poorly known. To test whether biogeographic boundaries influence the diversity and composition of host-associated microbiota, we analysed the microbiomes of three species of common intertidal gastropods at two sites separated by the biogeographic boundary at Point Conception (PtC), CA, using 16S rRNA gene sequencing. Our results show that each host species shows microbiome compositional specificity, even across PtC, and that alpha diversity does not change significantly across this boundary for any of the gastropod hosts. However, for two of the host species, beta diversity differs significantly across PtC, indicating that there may be multiple levels of organization of the marine gastropod microbiome. Overall, our results suggest that while biogeographic boundaries do not constrain the distribution of a core set of microbes associated with each host species, they can play a role in structuring the transient portion of the microbiome.

Loss of Biodiversity Dimensions through Shifting Climates and Ancient Mass Extinctions.

Many aspects of climate affect the deployment of biodiversity in time and space, and so changes in climate might be expected to drive regional and global extinction of both taxa and their ecological functions. Here we examine the association of past climate changes with extinction in marine bivalves, which are increasingly used as a model system for macroecological and macroevolutionary analysis. Focusing on the Cenozoic Era (66 Myr ago to the present), we analyze extinction patterns in shallow-water marine bivalve genera relative to temperature dynamics as estimated from isotopic data in microfossils. When the entire Cenozoic timeseries is considered, extinction intensity is not significantly associated with the mean temperature or the detrended variance in temperature within a given time interval (stratigraphic stage). However, extinction increases significantly with both the rate of temperature change within the stage of extinction and the absolute change in mean temperature from the preceding stage to the stage of extinction. Thus, several extinction events, particularly the extinction pulse near the Pliocene-Pleistocene boundary, do appear to have climatic drivers. Further, the latitudinal diversity gradient today and the Cenozoic history of polar faunas suggest that long-term, regional extinctions associated with cooling removed not just taxa but a variety of ecological functions from high-latitude seas. These dynamics of biodiversity loss contrast with the two mass extinctions bracketing the Mesozoic Era, which had negligible effects on the diversity of ecological functions despite removing nearly as many taxa as the latitudinal gradient does today. Thus, the fossil record raises a key issue: whether the biotic consequences of present-day stresses will more closely resemble the long-term effects of past climate changes or those that cascaded from the mass extinctions.

The origin and evolution of coral species richness in a marine biodiversity hotspot.

The Coral Triangle (CT) region of the Indo-Pacific realm harbors an extraordinary number of species, with richness decreasing away from this biodiversity hotspot. Despite multiple competing hypotheses, the dynamics underlying this regional diversity pattern remain poorly understood. Here, we use a time-calibrated evolutionary tree of living reef coral species, their current geographic ranges, and model-based estimates of regional rates of speciation, extinction, and geographic range shifts to show that origination rates within the CT are lower than in surrounding regions, a result inconsistent with the long-standing center of origin hypothesis. Furthermore, endemism of coral species in the CT is low, and the CT endemics are older than relatives found outside this region. Overall, our model results suggest that the high diversity of reef corals in the CT is largely due to range expansions into this region of species that evolved elsewhere. These findings strongly support the notion that geographic range shifts play a critical role in generating species diversity gradients. They also show that preserving the processes that gave rise to the striking diversity of corals in the CT requires protecting not just reefs within the hotspot, but also those in the surrounding areas.

Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography.

A latitudinal gradient in biodiversity has existed since before the time of the dinosaurs, yet how and why this gradient arose remains unresolved. Here we review two major hypotheses for the origin of the latitudinal diversity gradient. The time and area hypothesis holds that tropical climates are older and historically larger, allowing more opportunity for diversification. This hypothesis is supported by observations that temperate taxa are often younger than, and nested within, tropical taxa, and that diversity is positively correlated with the age and area of geographical regions. The diversification rate hypothesis holds that tropical regions diversify faster due to higher rates of speciation (caused by increased opportunities for the evolution of reproductive isolation, or faster molecular evolution, or the increased importance of biotic interactions), or due to lower extinction rates. There is phylogenetic evidence for higher rates of diversification in tropical clades, and palaeontological data demonstrate higher rates of origination for tropical taxa, but mixed evidence for latitudinal differences in extinction rates. Studies of latitudinal variation in incipient speciation also suggest faster speciation in the tropics. Distinguishing the roles of history, speciation and extinction in the origin of the latitudinal gradient represents a major challenge to future research.

Origination, extinction, and dispersal: integrative models for understanding present-day diversity gradients.

Species diversity gradients seen today are, to a large degree, a product of history. Spatially nonrandom originations, extinctions, and changes in geographic distributions can create gradients in species and higher-taxon richness, but the relative roles of each of these processes remain poorly documented. Existing explanations of diversity gradients have tended to focus on either macroevolutionary or biogeographic processes; integrative models that include both are largely lacking. We used simple models that incorporate origination and extinction rates along with dispersal of taxa between regions to show that dispersal not only affects regional richness patterns but also has a strong influence on the average age of taxa present in a region. Failure to take into account the effects of dispersal can, in principle, lead to biased estimates of diversification rates and potentially wrong conclusions regarding processes driving latitudinal and other gradients in diversity. Thus, it is critical to include the effects of dispersal when formulating and testing hypotheses about the causes of large-scale gradients in diversity. Finally, the model results, in conjunction with the results of existing empirical studies, suggest that the nature of macroevolutionary and biogeographic processes may differ between terrestrial and marine diversity gradients.