Contrasting responses of functional diversity to major losses in taxonomic diversity.

Taxonomic diversity of benthic marine invertebrate shelf species declines at present by nearly an order of magnitude from the tropics to the poles in each hemisphere along the latitudinal diversity gradient (LDG), most steeply along the western Pacific where shallow-sea diversity is at its tropical maximum. In the Bivalvia, a model system for macroevolution and macroecology, this taxonomic trend is accompanied by a decline in the number of functional groups and an increase in the evenness of taxa distributed among those groups, with maximum functional evenness (FE) in polar waters of both hemispheres. In contrast, analyses of this model system across the two era-defining events of the Phanerozoic, the Permian-Triassic and Cretaceous-Paleogene mass extinctions, show only minor declines in functional richness despite high extinction intensities, resulting in a rise in FE owing to the persistence of functional groups. We hypothesize that the spatial decline of taxonomic diversity and increase in FE along the present-day LDG primarily reflect diversity-dependent factors, whereas retention of almost all functional groups through the two mass extinctions suggests the operation of diversity-independent factors. Comparative analyses of different aspects of biodiversity thus reveal strongly contrasting biological consequences of similarly severe declines in taxonomic diversity and can help predict the consequences for functional diversity among different drivers of past, present, and future biodiversity loss.

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.

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.

Origination and immigration drive latitudinal gradients in marine functional diversity.

Global patterns in the functional attributes of organisms are critical to understanding biodiversity trends and predicting biotic responses to environmental change. In the first global marine analysis, we find a strong decrease in functional richness, but a strong increase in functional evenness, with increasing latitude using intertidal-to-outer-shelf bivalves as a model system (N = 5571 species). These patterns appear to be driven by the interplay between variation in origination rates among functional groups, and latitudinal patterns in origination and range expansion, as documented by the rich fossil record of the group. The data suggest that (i) accumulation of taxa in spatial bins and functional categories has not impeded continued diversification in the tropics, and (ii) extinctions will influence ecosystem function differentially across latitudes.

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.

Genus age, provincial area and the taxonomic structure of marine faunas.

Species are unevenly distributed among genera within clades and regions, with most genera species-poor and few species-rich. At regional scales, this structure to taxonomic diversity is generated via speciation, extinction and geographical range dynamics. Here, we use a global database of extant marine bivalves to characterize the taxonomic structure of climate zones and provinces. Our analyses reveal a general, Zipf-Mandelbrot form to the distribution of species among genera, with faunas from similar climate zones exhibiting similar taxonomic structure. Provinces that contain older taxa and/or encompass larger areas are expected to be more species-rich. Although both median genus age and provincial area correlate with measures of taxonomic structure, these relationships are interdependent, nonlinear and driven primarily by contrasts between tropical and extra-tropical faunas. Provincial area and taxonomic structure are largely decoupled within climate zones. Counter to the expectation that genus age and species richness should positively covary, diverse and highly structured provincial faunas are dominated by young genera. The marked differences between tropical and temperate faunas suggest strong spatial variation in evolutionary rates and invasion frequencies. Such variation contradicts biogeographic models that scale taxonomic diversity to geographical area.

The importance of preadapted genomes in the origin of the animal bodyplans and the Cambrian explosion.

The genomes of taxa whose stem lineages branched early in metazoan history, and of allied protistan groups, provide a tantalizing outline of the morphological and genomic changes that accompanied the origin and early diversifications of animals. Genome comparisons show that the early clades increasingly contain genes that mediate development of complex features only seen in later metazoan branches. Peak additions of protein-coding regulatory genes occurred deep in the metazoan tree, evidently within stem groups of metazoans and eumetazoans. However, the bodyplans of these early-branching clades are relatively simple. The existence of major elements of the bilaterian developmental toolkit in these simpler organisms implies that these components evolved for functions other than the production of complex morphology, preadapting the genome for the morphological differentiation that occurred higher in metazoan phylogeny. Stem lineages of the bilaterian phyla apparently required few additional genes beyond their diploblastic ancestors. As disparate bodyplans appeared and diversified during the Cambrian explosion, increasing complexity was accommodated largely through changes in cis-regulatory networks, accompanied by some additional gene novelties. Subsequently, protein-coding genic richness appears to have essentially plateaued. Some genomic evidence suggests that similar stages of genomic evolution may have accompanied the rise of land plants.

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.

Signature of the end-Cretaceous mass extinction in the modern biota.

The long-term effects of mass extinctions on spatial and evolutionary dynamics have been poorly studied. Here we show that the evolutionary consequences of the end-Cretaceous [Cretaceous/Paleogene (K/Pg)] mass extinction persist in present-day biogeography. The geologic ages of genera of living marine bivalves show a significant break from a smooth exponential distribution, corresponding to the K/Pg boundary. The break reflects a permanent increase in origination rates, intermediate between the Mesozoic rate and the post-extinction recovery pulse. This global rate shift is most clearly seen today in tropical bioprovinces and weakens toward the poles. Coupled with the modern geographic distributions of taxa originating before and after the K/Pg boundary, this spatial pattern indicates that tropical origination rates after the K/Pg event have left a permanent mark on the taxonomic and biogeographic structure of the modern biota, despite the complex Cenozoic history of marine environments.

Generation of Earth's first-order biodiversity pattern.

The first-order biodiversity pattern on Earth today and at least as far back as the Paleozoic is the latitudinal diversity gradient (LDG), a decrease in richness of species and higher taxa from the equator to the poles. LDGs are produced by geographic trends in origination, extinction, and dispersal over evolutionary timescales, so that analyses of static patterns will be insufficient to reveal underlying processes. The fossil record of marine bivalve genera, a model system for the analysis of biodiversity dynamics over large temporal and spatial scales, shows that an origination and range-expansion gradient plays a major role in generating the LDG. Peak origination rates and peak diversities fall within the tropics, with range expansion out of the tropics the predominant spatial dynamic thereafter. The origination-diversity link occurs even in a "contrarian" group whose diversity peaks at midlatitudes, an exception proving the rule that spatial variations in origination are key to latitudinal diversity patterns. Extinction rates are lower in polar latitudes (> or =60 degrees ) than in temperate zones and thus cannot create the observed gradient alone. They may, however, help to explain why origination and immigration are evidently damped in higher latitudes. We suggest that species require more resources in higher latitudes, for the seasonality of primary productivity increases by more than an order of magnitude from equatorial to polar regions. Higher-latitude species are generalists that, unlike potential immigrants, are adapted to garner the large share of resources required for incumbency in those regions. When resources are opened up by extinctions, lineages spread chiefly poleward and chiefly through speciation.

Species-genus ratios reflect a global history of diversification and range expansion in marine bivalves.

The distribution of marine bivalve species among genera and higher taxa takes the form of the classic hollow curve, wherein few lineages are species rich and many are species poor. The distribution of species among genera (S/G ratio) varies with latitude, with temperate S/G's falling within the null expectation, and tropical and polar S/G's exceeding it. Here, we test several hypotheses for this polar overdominance in the species richness of small numbers of genera. We find a significant positive correlation between the latitudinal range of a genus and its species richness, both globally and within regions. Genus age and species richness are also positively related, but this relationship breaks down when the analysis is limited to genera endemic to climate zones or with narrow latitudinal ranges. The data suggest a link between speciation and range-expansion, with genera expanding out of the tropical latitudinal bins tending to speciate more prolifically, both globally and regionally. These genera contain more species within climate zones than taxa endemic to that zone. Range expansion thus appears to be fundamentally coupled with speciation, producing the skewed distribution of species among genera, both globally and regionally, whereas clade longevity is achieved through extinction -- resistance conferred by broad geographical ranges.

Contrarian clade confirms the ubiquity of spatial origination patterns in the production of latitudinal diversity gradients.

The latitudinal diversity gradient (LDG), wherein the number of species and higher taxa peaks in the tropics and decreases toward the poles, is the best-documented large-scale diversity pattern on Earth, but hypotheses explaining the standard LDG must also account for rare "contrarian" taxa that show diversity maxima outside of the tropics. For marine bivalves, one of the few groups that provide spatially explicit temporal data on a global scale, we show that a major contrarian group, the Anomalodesmata, unexpectedly exhibits the same large-scale dynamics as related clades having normal LDGs in two key respects. First, maxima in standing genus diversity and genus origination rates coincide spatially. Second, the strength of a clade's present-day LDG is significantly related to the proportion of its living genera that originated in the tropics during the late Cenozoic, with the contrarian gradient strength at both species and genus level predicted quantitatively by the values for the other clades. Geologic age distributions indicate that the anomalous LDG results from origination that is damped in the tropics rather than heightened in the temperate zones. The pervasive role of spatial origination patterns in shaping LDGs, regardless of the position of their diversity maxima, corroborates hypotheses based on clades showing standard gradients and underscores the insights that contrarian groups can provide into general principles of diversity dynamics.

Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient.

The evolutionary dynamics underlying the latitudinal gradient in biodiversity have been controversial for over a century. Using a spatially explicit approach that incorporates not only origination and extinction but immigration, a global analysis of genera and subgenera of marine bivalves over the past 11 million years supports an "out of the tropics" model, in which taxa preferentially originate in the tropics and expand toward the poles without losing their tropical presence. The tropics are thus both a cradle and a museum of biodiversity, contrary to the conceptual dichotomy dominant since 1974; a tropical diversity crisis would thus have profound evolutionary effects at all latitudes.

Assessing the fidelity of the fossil record by using marine bivalves.

Taxa that fail to become incorporated into the fossil record can reveal much about the biases of this record and provide the information needed to correct such biases in empirical analyses of the history of life. Yet little is known about the characteristics of taxa missing from the fossil record. For the marine Bivalvia, which have become a model system for macroevolutionary and macroecological analysis in the fossil record, 308 of the 1,292 living genera and subgenera (herein termed "taxa") are not recorded as fossils. These missing taxa are not a random sample of the clade, but instead tend to have small body size, reactive shell structures, commensal or parasitic habit, deep-sea distribution, narrow geographic range, restriction to regions exposing few Neogene marine sediments, or recent date of formal taxonomic description in the neontological literature. Most missing taxa show two or more of these features and tend to be concentrated in particular families. When we exclude the smallest taxa (<1 cm) and deep-sea endemics, date of published description and geographic range become the strongest predictors of the missing taxa; other factors are statistically insignificant or have relatively small effects. These biases might influence a variety of analyses including the use of fossil data in support of phylogenetic analyses, molecular clock calibrations, and analyses of spatial and temporal dynamics of clades and biotas. Clade inventories such as these can be used to develop protocols that minimize the biases imposed by sampling and preservation.

The impact of the pull of the recent on the history of marine diversity.

Up to 50% of the increase in marine animal biodiversity through the Cenozoic at the genus level has been attributed to a sampling bias termed "the Pull of the Recent," the extension of stratigraphic ranges of fossil taxa by the relatively complete sampling of the Recent biota. However, 906 of 958 living genera and subgenera of bivalve mollusks having a fossil record occur in the Pliocene or Pleistocene. The Pull of the Recent thus accounts for only 5% of the Cenozoic increase in bivalve diversity, a major component of the marine record, suggesting that the diversity increase is likely to be a genuine biological pattern.

Architectures of biological complexity.

Three features contribute to the complexity of an entity: number of parts, their order, and their iteration. Many functional biological entities are complex when measured by those attributes, and although they are produced in tree-like architectures, the organizational structures that permit them to function are in the form of hierarchies. Natural hierarchies can be thought of as organizing structures that are emergent properties of complex functional entities, and which are transformed from trees by process networks. For example, hierarchies are observed in the architecture of metazoan bodies (the somatic hierarchy) and in the biotic structure of ecogeographic units (the ecological hierarchy). As the metazoan developmental genome is quite complex and has been evolved through tree-like processes, it must harbor at least one hierarchy, which is most clearly indicated in the developmental processes that create the somatic hierarchy. For multicellular organisms, the processes that serve to transform trees of gene expression events into a somatic hierarchy have produced complicated signaling networks whose histories can probably be recovered in general outline.

Morphological and developmental macroevolution: a paleontological perspective.

Evidence of the morphological evolution of metazoans has been preserved, in varying degrees of completeness, in the fossil record of the last 600 million years. Although extinction has been incessant at lower taxonomic levels, genomic comparisons among surviving members of higher taxa suggest that much of the developmental systems that pattern their bodyplans has been conserved from early in their history. Comparisons between the origin of morphological disparity in the record and patterns of genomic disparity among living taxa promise to be interesting. For example, Hox cluster composition varies among major taxa, and the fossil record suggests that many of the changes in Hox clusters may have been associated with late Neoproterozoic evolution among minute benthic vermiform clades, from which crown bilaterian phyla arose just before or during the Cambrian explosion. Study of genomic differences among crown classes and orders whosetiming and mode of origin can be inferred from morphological data inthefossil record should throw further light on the timing and mode of origin of genomic disparities.