High male sexual investment as a driver of extinction in fossil ostracods.

Sexual selection favours traits that confer advantages in the competition for mates. In many cases, such traits are costly to produce and maintain, because the costs help to enforce the honesty of these signals and cues 1 . Some evolutionary models predict that sexual selection also produces costs at the population level, which could limit the ability of populations to adapt to changing conditions and thus increase the risk of extinction2-4. Other models, however, suggest that sexual selection should increase rates of adaptation and enhance the removal of deleterious mutations, thus protecting populations against extinction3, 5, 6. Resolving the conflict between these models is not only important for explaining the history of biodiversity, but also relevant to understanding the mechanisms of the current biodiversity crisis. Previous attempts to test the conflicting predictions produced by these models have been limited to extant species and have thus relied on indirect proxies for species extinction. Here we use the informative fossil record of cytheroid ostracods-small, bivalved crustaceans with sexually dimorphic carapaces-to test how sexual selection relates to actual species extinction. We show that species with more pronounced sexual dimorphism, indicating the highest levels of male investment in reproduction, had estimated extinction rates that were ten times higher than those of the species with the lowest investment. These results indicate that sexual selection can be a substantial risk factor for extinction.

Shifts in sexual dimorphism across a mass extinction in ostracods: implications for sexual selection as a factor in extinction risk.

Sexual selection often favours investment in expensive sexual traits that help individuals compete for mates. In a rapidly changing environment, however, allocation of resources to traits related to reproduction at the expense of those related to survival may elevate extinction risk. Empirical testing of this hypothesis in the fossil record, where extinction can be directly documented, is largely lacking. The rich fossil record of cytheroid ostracods offers a unique study system in this context: the male shell is systematically more elongate than that of females, and thus the sexes can be distinguished, even in fossils. Using mixture models to identify sex clusters from size and shape variables derived from the digitized valve outlines of adult ostracods, we estimated sexual dimorphism in ostracod species before and after the Cretaceous/Palaeogene mass extinction in the United States Coastal Plain. Across this boundary, we document a substantial shift in sexual dimorphism, driven largely by a pronounced decline in the taxa with dimorphism indicating both very high and very low male investment. The shift away from high male investment, which arises largely from evolutionary changes within genera that persist through the extinction, parallels extinction selectivity previously documented during the Late Cretaceous under a background extinction regime. Our results suggest that sexual selection and the allocation of resources towards survival versus reproduction may be an important factor for species extinction during both background and mass extinctions.

Sex and the shifting biodiversity dynamics of marine animals in deep time.

The fossil record of marine animals suggests that diversity-dependent processes exerted strong control on biodiversification: after the Ordovician Radiation, genus richness did not trend for hundreds of millions of years. However, diversity subsequently rose dramatically in the Cretaceous and Cenozoic (145 million years ago-present), indicating that limits on diversification can be overcome by ecological or evolutionary change. Here, we show that the Cretaceous-Cenozoic radiation was driven by increased diversification in animals that transfer sperm between adults during fertilization, whereas animals that broadcast sperm into the water column have not changed significantly in richness since the Late Ordovician (∼450 million years ago). We argue that the former group radiated in part because directed sperm transfer permits smaller population sizes and additional modes of prezygotic isolation, as has been argued previously for the coincident radiation of angiosperms. Directed sperm transfer tends to co-occur with many ecological traits, such as a predatory lifestyle. Ecological specialization likely operated synergistically with mode of fertilization in driving the diversification that began during the Mesozoic marine revolution. Plausibly, the ultimate driver of diversification was an increase in food availability, but its effects on the fauna were regulated by fundamental reproductive and ecological traits.

Two pulses of morphological diversification in Pacific pelagic fishes following the Cretaceous-Palaeogene mass extinction.

Molecular phylogenies suggest some major radiations of open-ocean fish clades occurred roughly coincident with the Cretaceous-Palaeogene (K/Pg) boundary, however the timing and nature of this diversification is poorly constrained. Here, we investigate evolutionary patterns in ray-finned fishes across the K/Pg mass extinction 66 million years ago (Ma), using microfossils (isolated teeth) preserved in a South Pacific sediment core spanning 72-43 Ma. Our record does not show significant turnover of fish tooth morphotypes at the K/Pg boundary: only two of 48 Cretaceous tooth morphotypes disappear at the event in the South Pacific, a rate no different from background extinction. Capture-mark-recapture analysis finds two pulses of origination in fish tooth morphotypes following the mass extinction. The first pulse, at approximately 64 Ma, included short-lived teeth, as well as forms that contribute to an expansion into novel morphospace. A second pulse, centred at approximately 58 Ma, produced morphotype novelty in a different region of morphospace from the first pulse, and contributed significantly to Eocene tooth morphospace occupation. There was no significant increase in origination rates or expansion into novel morphospace during the early or middle Eocene, despite a near 10-fold increase in tooth abundance during that interval. Our results suggest that while the K/Pg event had a minor impact on fish diversity in terms of extinction, the removal of the few dominant Cretaceous morphotypes triggered a sequence of origination events allowing fishes to rapidly diversify morphologically, setting the stage for exceptional levels of ray-finned fish diversity in the Cenozoic.

Simple versus complex models of trait evolution and stasis as a response to environmental change.

Previous analyses of evolutionary patterns, or modes, in fossil lineages have focused overwhelmingly on three simple models: stasis, random walks, and directional evolution. Here we use likelihood methods to fit an expanded set of evolutionary models to a large compilation of ancestor-descendant series of populations from the fossil record. In addition to the standard three models, we assess more complex models with punctuations and shifts from one evolutionary mode to another. As in previous studies, we find that stasis is common in the fossil record, as is a strict version of stasis that entails no real evolutionary changes. Incidence of directional evolution is relatively low (13%), but higher than in previous studies because our analytical approach can more sensitively detect noisy trends. Complex evolutionary models are often favored, overwhelmingly so for sequences comprising many samples. This finding is consistent with evolutionary dynamics that are, in reality, more complex than any of the models we consider. Furthermore, the timing of shifts in evolutionary dynamics varies among traits measured from the same series. Finally, we use our empirical collection of evolutionary sequences and a long and highly resolved proxy for global climate to inform simulations in which traits adaptively track temperature changes over time. When realistically calibrated, we find that this simple model can reproduce important aspects of our paleontological results. We conclude that observed paleontological patterns, including the prevalence of stasis, need not be inconsistent with adaptive evolution, even in the face of unstable physical environments.

Morphological stasis in an ongoing gastropod radiation from Lake Malawi.

Evolutionary processes leading to adaptive radiation regularly occur too fast to be accurately recorded in the fossil record but too slowly to be readily observed in living biota. The study of evolutionary radiations is thereby confronted with an epistemological gap between the timescales and approaches used by neontologists and paleontologists. Here we report on an ongoing radiation of extant Bellamya species (n = 4) from the African Rift Lake Malawi that provides an unusual opportunity to bridge this gap. The substantial molecular differentiation in this monophyletic Bellamya clade has arisen since Late Pleistocene megadroughts in the Malawi Basin caused by climate change. Morphological time-series analysis of a high-resolution, radiocarbon-dated sequence of 22 faunas spanning the Holocene documents stasis up to the middle Holocene in all traits studied (shell height, number of whorls, and two variables obtained from geometric morphometrics). Between deposition of the last fossil fauna (~5 ka) and the present day, a drastic increase in morphological disparity was observed (3.7-5.8 times) associated with an increase in species diversity. Comparison of the rates of morphological evolution obtained from the paleontological time-series with phylogenetic rates indicates that the divergence in two traits could be reconstructed with the slow rates documented in the fossils, that one trait required a rate reduction (stabilizing selection), and the other faster rates (divergent selection). The combined paleontological and comparative approach taken here allows recognition that morphological stasis can be the dominant evolutionary pattern within species lineages, even in very young and radiating clades.

Cross-disciplinary information for understanding macroevolution.

Many different macroevolutionary models can produce the same observations. Despite efforts in building more complex and realistic models, it may still be difficult to distinguish the processes that have generated the biodiversity we observe. In this opinion we argue that we can make new progress by reaching out across disciplines, relying on independent data and theory to constrain macroevolutionary inference. Using mainly paleontological insights and data, we illustrate how we can eliminate less plausible or implausible models, and/or parts of parameter space, while applying comparative phylogenetic approaches. We emphasize that such cross-disciplinary insights and data can be drawn between many other disciplines relevant to macroevolution. We urge cross-disciplinary training, and collaboration using common-use databases as a platform for increasing our understanding.

Latitudinal species diversity gradient of marine zooplankton for the last three million years.

High tropical and low polar biodiversity is one of the most fundamental patterns characterising marine ecosystems, and the influence of temperature on such marine latitudinal diversity gradients is increasingly well documented. However, the temporal stability of quantitative relationships among diversity, latitude and temperature is largely unknown. Herein we document marine zooplankton species diversity patterns at four time slices [modern, Last Glacial Maximum (18,000 years ago), last interglacial (120,000 years ago), and Pliocene (~3.3-3.0 million years ago)] and show that, although the diversity-latitude relationship has been dynamic, diversity-temperature relationships are remarkably constant over the past three million years. These results suggest that species diversity is rapidly reorganised as species' ranges respond to temperature change on ecological time scales, and that the ecological impact of future human-induced temperature change may be partly predictable from fossil and paleoclimatological records.

Temporal latitudinal-gradient dynamics and tropical instability of deep-sea species diversity.

A benthic microfaunal record from the equatorial Atlantic Ocean over the past four glacial-interglacial cycles was investigated to understand temporal dynamics of deep-sea latitudinal species diversity gradients (LSDGs). The results demonstrate unexpected instability and high amplitude fluctuations of species diversity in the tropical deep ocean that are correlated with orbital-scale oscillations in global climate: Species diversity is low during glacial and high during interglacial periods. This implies that climate severely influences deep-sea diversity, even at tropical latitudes, and that deep-sea LSDGs, while generally present for the last 36 million years, were weakened or absent during glacial periods. Temporally dynamic LSDGs and unstable tropical diversity require reconsideration of current ecological hypotheses about the generation and maintenance of biodiversity as they apply to the deep sea, and underscore the potential vulnerability and conservation importance of tropical deep-sea ecosystems.

A fossil record of developmental events: variation and evolution in epidermal cell divisions in ostracodes.

The carapaces of some ostracode taxa bear reticulate skeletal ridges that outline underlying epidermal cells. This anatomy allows one to identify homologous cells across individuals, to infer the modal sequence of cell divisions that occurs over ontogeny, and to identify individuals with variant cell patterns (e.g., additional or missing cell divisions), even in fossils. Here we explore the variational properties and evolutionary history of this developmental system in the deep-sea ostracode genus Poseidonamicus. Using a sample of over 2000 specimens to capture variation in cell division sequence, we show that phenotypic variation in this system is highly structured: some variants, regions of the carapace, and lineages are much more variable than others. Much of the differences in variation among cells can be attributed to the molt stage in which cells take their final form-cell divisions occurring later in ontogeny are more variable than those earlier. Despite ample variation, only two evolutionary changes in the sequence of cell divisions occur over the 40 Myr history of this clade. The evolutionary changes that do occur parallel the two most common intraspecific variants, suggesting that developmental structuring of variation can have long-term evolutionary consequences. Analysis of the most common variant over the last two molt stages suggests that it suffers a fitness disadvantage relative to the modal form. Such normalizing selection may contribute to the evolutionary conservativeness of this developmental system in the Ostracoda.

Evolution in fossil lineages: paleontology and The Origin of Species.

Of all of the sources of evidence for evolution by natural selection, perhaps the most problematic for Darwin was the geological record of organic change. In response to the absence of species-level transformations in the fossil record, Darwin argued that the fossil record was too incomplete, too biased, and too poorly known to provide strong evidence against his theory. Here, this view of the fossil record is evaluated in light of 150 years of subsequent paleontological research. Although Darwin's assessment of the completeness and resolution of fossiliferous rocks was in several ways astute, today the fossil record is much better explored, documented, and understood than it was in 1859. In particular, a reasonably large set of studies tracing evolutionary trajectories within species can now be brought to bear on Darwin's expectation of gradual change driven by natural selection. An unusually high-resolution sequence of stickleback-bearing strata records the transformation of this lineage via natural selection. This adaptive trajectory is qualitatively consistent with Darwin's prediction, but it occurred much more rapidly than he would have guessed: almost all of the directional change was completed within 1,000 generations. In most geological sequences, this change would be too rapid to resolve. The accumulated fossil record at more typical paleontological scales (10(4)-10(6) years) reveals evolutionary changes that are rarely directional and net rates of change that are perhaps surprisingly slow, two findings that are in agreement with the punctuated-equilibrium model. Finally, Darwin's view of the broader history of life is reviewed briefly, with a focus on competition-mediated extinction and recent paleontological and phylogenetic attempts to assess diversity dependence in evolutionary dynamics.

The relative importance of directional change, random walks, and stasis in the evolution of fossil lineages.

The nature of evolutionary changes recorded by the fossil record has long been controversial, with particular disagreement concerning the relative frequency of gradual change versus stasis within lineages. Here, I present a large-scale, statistical survey of evolutionary mode in fossil lineages. Over 250 sequences of evolving traits were fit by using maximum likelihood to three evolutionary models: directional change, random walk, and stasis. Evolution in these traits was rarely directional; in only 5% of fossil sequences was directional evolution the most strongly supported of the three modes of change. The remaining 95% of sequences were divided nearly equally between random walks and stasis. Variables related to body size were significantly less likely than shape traits to experience stasis. This finding is in accord with previous suggestions that size may be more evolutionarily labile than shape and is consistent with some but not all of the mechanisms proposed to explain evolutionary stasis. In general, similar evolutionary patterns are observed across other variables, such as clade membership and temporal resolution, but there is some evidence that directional change in planktonic organisms is more frequent than in benthic organisms. The rarity with which directional evolution was observed in this study corroborates a key claim of punctuated equilibria and suggests that truly directional evolution is infrequent or, perhaps more importantly, of short enough duration so as to rarely register in paleontological sampling.

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.

Taxonomy of Ostracods from the Pirabas Formation (Upper Oligocene to Lower Miocene), Eastern Amazonia (Pará State, Brazil).

Ostracods from the Upper Oligocene to Lower Miocene Pirabas Formation, Northeastern Amazonia, Pará State, Brazil were examined from one subsurface and four outcrop sections. A total of 119 species were recognized and are illustrated; another 53 species were left in open nomenclature. Twenty-seven of the species are common to the Neogene of Caribbean, another two species are known from areas other than the Caribbean, and one species was already described from the studied unit. This study provides a robust taxonomic database for paleoenvironmental, biostratigraphic and paleogeographic studies and contributes to the knowledge of the paleodiversity of Neogene Ostracods from the Southwestern Atlantic.

Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage.

Natural selection has almost certainly shaped many evolutionary trajectories documented in fossil lineages, but it has proven difficult to demonstrate this claim by analyzing sequences of evolutionary changes. In a recently published and particularly promising test case, an evolutionary time series of populations displaying armor reduction in a fossil stickleback lineage could not be consistently distinguished from a null model of neutral drift, despite excellent temporal resolution and an abundance of indirect evidence implicating natural selection. Here, we revisit this case study, applying analyses that differ from standard approaches in that: (1) we do not treat genetic drift as a null model, and instead assess neutral and adaptive explanations on equal footing using the Akaike Information Criterion; and (2) rather than constant directional selection, the adaptive scenario we consider is that of a population ascending a peak on the adaptive landscape, modeled as an Orstein-Uhlenbeck process. For all three skeletal features measured in the stickleback lineage, the adaptive model decisively outperforms neutral evolution, supporting a role for natural selection in the evolution of these traits. These results demonstrate that, at least under favorable circumstances, it is possible to infer in fossil lineages the relationship between evolutionary change and features of the adaptive landscape.

Evolutionary divergence in directions of high phenotypic variance in the ostracode genus poseidonamicus.

Trait variation and covariation are understood to influence the response of populations to natural selection on generational time scales, but their role, if any, in shaping long-term macroevolutionary divergence is still unclear. The present study uses the rich fossil record of the ostracode genus Poseidonamicus to reconstruct in great detail the evolutionary history of a set of landmark-based morphometric characters. This reconstruction included two kinds of evolutionary inferences: ancestor-descendant transitions among populations repeatedly sampled at the same location and divergence between lineages measured as independent contrasts on a phylogeny. This reconstructed history was then used to test if evolutionary changes were concentrated in directions (traits or combinations of traits) with high phenotypic variance. Two different statistics of association between evolution and variation tested the null hypothesis that evolutionary changes occur in random directions with respect to trait variability. The first of these measured the similarity between the directions of evolutionary change and the axis of maximum variance, and the second measured the degree to which evolutionary changes were concentrated in directions of high phenotypic variation. Randomization tests indicated that both kinds of evolutionary inferences (ancestor-descendant and phylogenetic contrasts) occurred preferentially in directions of high phenotypic variance (and close to the axis of maximal variation), suggesting that within-population variation can structure long-term divergence. This effect decayed after a few million years, but at least for one metric, never disappeared completely. These results are consistent with Schluter's genetic constraints model in which evolutionary trajectories on adaptive landscapes are deflected by variation within and covariation among traits.

A novel crustacean swimming stroke: coordinated four-paddled locomotion in the cypridoidean ostracode Cypridopsis vidua (Müller).

Despite the diversity and ecological importance of cypridoidean ostracodes, there have been no kinematic studies of how they swim. We used regular and high-speed video of tethered ostracodes to document locomotion in the cypridoidean species Cypridopsis vidua. Swimming in this species is drag-based, with thrust provided by both antennulae and antennae. About 15 complete power and recovery strokes occur per second; maximal speeds for the limb tips were about 30 mm/s for the antennulae and 50 mm/s for the antennae. These speeds correspond to Reynolds numbers on the order of 10(-1) to 10(0) for the limb tips and 10(-2) to 10(-1) for the setae that extend outward from the swimming limbs and provide much of the surface area of the limb. The strokes of the four thrust-producing limbs are coordinated in a manner that seems to be unique among aquatic arthropods. When viewed from the anterior, power strokes are synchronized diagonally: left antennula and right antenna power strokes start at the same time and terminate just as the power strokes for the right antennula and left antenna begin. Because power strokes occur throughout the stroke cycle, swimming in this species is smoothly continuous, without the rapid accelerations and decelerations characteristic of most small aquatic arthropods.

Correlation between investment in sexual traits and valve sexual dimorphism in Cyprideis species (Ostracoda).

Assessing the long-term macroevolutionary consequences of sexual selection has been hampered by the difficulty of studying this process in the fossil record. Cytheroid ostracodes offer an excellent system to explore sexual selection in the fossil record because their readily fossilized carapaces are sexually dimorphic. Specifically, males are relatively more elongate than females in this superfamily. This sexual shape difference is thought to arise so that males carapaces can accommodate their very large copulatory apparatus, which can account for up to one-third of body volume. Here we test this widely held explanation for sexual dimorphism in cytheroid ostracodes by correlating investment in male genitalia, a trait in which sexual selection is seen as the main evolutionary driver, with sexual dimorphism of carapace in the genus Cyprideis. We analyzed specimens collected in the field (C. salebrosa, USA; C. torosa, UK) and from collections of the National Museum of Natural History, Washington, DC (C. mexicana). We digitized valve outlines in lateral view to obtain measures of size (valve area) and shape (elongation, measured as length to height ratio), and obtained several dimensions from two components of the hemipenis: the muscular basal capsule, which functions as a sperm pump, and the section that includes the intromittent organ (terminal extension). In addition to the assessment of this primary sexual trait, we also quantified two dimensions of the male secondary sexual trait-where the transformed right walking leg functions as a clasping organ during mating. We also measured linear dimensions from four limbs as indicators of overall (soft-part) body size, and assessed allometry of the soft anatomy. We observed significant correlations in males between valve size, but not elongation, and distinct structural parts of the hemipenis, even after accounting for their shared correlation with overall body size. We also found weak but significant positive correlation between valve elongation and the degree of sexual dimorphism of the walking leg, but only in C. torosa. The correlation between the hemipenis parts, especially basal capsule size and male valve size dimorphism suggests that sexual selection on sperm size, quantity, and/or efficiency of transfer may drive sexual size dimorphism in these species, although we cannot exclude other aspects of sexual and natural selection.