Wild pedigrees inform mutation rates and historic abundance in baleen whales.

Phylogeny-based estimates suggesting a low germline mutation rate (µ) in baleen whales have influenced research ranging from assessments of whaling impacts to evolutionary cancer biology. We estimated µ directly from pedigrees in four baleen whale species for both the mitochondrial control region and nuclear genome. The results suggest values higher than those obtained through phylogeny-based estimates and similar to pedigree-based values for primates and toothed whales. Applying our estimate of µ reduces previous genetic-based estimates of preexploitation whale abundance by 86% and suggests that µ cannot explain low cancer rates in gigantic mammals. Our study shows that it is feasible to estimate µ directly from pedigrees in natural populations, with wide-ranging implications for ecological and evolutionary research.

Social modulation of oogenesis and egg laying in Drosophila melanogaster.

Being part of a group facilitates cooperation between group members but also creates competition for resources. This is a conundrum for gravid females, whose future offspring benefit from being in a group only if there are enough resources relative to group size. Females may therefore be expected to modulate reproductive output depending on social context. In the fruit fly Drosophila melanogaster, females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The genetic tractability of this species allows dissecting the mechanisms underlying physiological adaptation to social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster when grouped than when isolated, females reduce competition between offspring and increase offspring survival. In addition, grouped females lay eggs during the day, while isolated females lay them at night. We show that responses to the presence of others requires visual input and that flies from any sex, mating status, or species can trigger these responses. The mechanisms of this modulation of egg laying by group is connected to a lifting of the inhibition of light on oogenesis and egg laying, possibly mediated in part by an increase in juvenile hormone activity. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings in a species considered solitary question the validity of this nomenclature and suggest a widespread and profound influence of social context on reproduction.

Evolutionary radiation in canids following continental colonizations.

Colonization of a new environment may trigger an evolutionary radiation, defined as an accelerated accumulation of species in a short period of time. However, how often colonization events trigger such radiations is still an open question. We studied the worldwide dispersal of Caninae to investigate whether the invasion of new continents resulted in elevated species diversification. We used a combination of ancestral range estimation and phylogenetic analyses to estimate the ancestral ranges of 56 extant and extinct species of Caninae, as well as variation in speciation and extinction rates through time and across clades. Our findings indicate that canids experienced an evolutionary radiation event when lineages were able to reach Eurasia and South America around 11 million years ago. A large number of species arising in a short period of time suggests that canids experienced ecological opportunity events within the new areas, implying that the differences in the ecological settings between continents, and size variation among Canidae and other carnivores may be responsible for the variation in clade dynamics. We suggest that the increase of grasslands and the new herbivorous fauna that came with it were the major forces responsible for the diversification of wolves in North America, while empty niches and the absence of competitors can explain the success of canids in Africa and South America. Interaction with other carnivores probably also affected the diversification dynamics of canids.

Can we ignore trait-dependent colonization and diversification in island biogeography?

The application of state-dependent speciation and extinction models to phylogenetic trees has shown an important role for traits in diversification. However, this role remains comparatively unexplored on islands, which can include multiple independent clades resulting from different colonization events. To explore whether assuming no dependence on traits leads to bias in inference on island dynamics, we extend an island biodiversity model, DAISIE (Dynamic Assembly of Islands through Speciation, Immigration, and Extinction) to include trait-dependent diversification simulations, and evaluate the robustness of the inference model which ignores this trait-dependence. Our results indicate that when the differences between colonization, extinction, and speciation rates between trait states are moderate, the model shows negligible error for a variety of island diversity metrics, suggesting that island diversity dynamics can be accurately estimated without the need to explicitly model trait dependence. We conclude that for many biologically realistic scenarios with trait-dependent diversification and colonization, this simple trait-less inference model is informative and robust to trait effects on colonization, speciation, and extinction. Nonetheless, our new simulation model may provide a useful tool for studying patterns of trait variation.

The Phylogenetic Limits to Diversity-Dependent Diversification.

While the theory of micro-evolution by natural selection assigns a crucial role to competition, its role in macroevolution is less clear. Phylogenetic evidence for a decelerating accumulation of lineages suggests a feedback of lineage diversity on diversification. However, does this feedback only occur between close relatives, or do distant relatives also influence each other's diversification? In other words: are there phylogenetic limits to this diversity-dependence? Islands form ideal systems to answer these questions because their boundedness facilitates an overview of all potential competitors. The DAISIE (Dynamic Assembly of Island biota through Speciation Immigration and Extinction) framework allows for testing the presence of diversity-dependence on islands given phylogenetic data on colonization and branching times. The current inference models in DAISIE assume that this diversity-dependence only applies within a colonizing clade, i.e., all mainland species can colonize and diversify independently from one another. We term this clade-specific (CS) diversity-dependence. Here we introduce a new DAISIE model that assumes that diversity-dependence applies to all island species of a taxonomic group regardless of their mainland ancestry, i.e., diversity-dependence applies both to species within the same clade and between different clades established by different mainland species. We call this island-wide (IW) diversity-dependence. We present a method to compute a likelihood for this model given phylogenetic data on colonization and branching events and use likelihood ratio bootstrapping to compare it to the likelihood of the CS model in order to overcome biases known for standard model selection. We apply it to the diversification of Eleutherodactylus frogs on Hispaniola. Across the Greater Antilles archipelago, this radiation shows repeated patterns of diversification in ecotypes that are similar across clades. This could be suggestive of overlapping niche space and hence between-clade interactions, i.e., IW diversity-dependence. But it could also be suggestive of only within-clade interactions because between-clade interactions would have blocked the same ecotype from re-appearing. We find that the CS model fits the data much better than the IW model, indicating that different colonizations while resulting in similar ecotypes, are sufficiently distinct to avoid interacting strongly. We argue that non-overlapping distributions between clades (both spatially and in terms of ecotypes) cannot be used as evidence of CS diversity-dependence, because this pattern may be a consequence of IW diversity-dependence. By contrast, by using phylogenetic data rather than distributional data our method does allow for inferring the phylogenetic limits to diversity-dependent diversification. We discuss possibilities for future extensions and applications of our modelling approach. [Adaptive radiation; birth-death model; Caribbean; diversity-dependence; Eleutherodactylus; island biogeography.].

Microbiome Heritability and Its Role in Adaptation of Hosts to Novel Resources.

Microbiomes are involved in most vital processes, such as immune response, detoxification, and digestion and are thereby elementary to organismal functioning and ultimately the host's fitness. In turn, the microbiome may be influenced by the host and by the host's environment. To understand microbiome dynamics during the process of adaptation to new resources, we performed an evolutionary experiment with the two-spotted spider mite, Tetranychus urticae. We generated genetically depleted strains of the two-spotted spider mite and reared them on their ancestral host plant and two novel host plants for approximately 12 generations. The use of genetically depleted strains reduced the magnitude of genetic adaptation of the spider mite host to the new resource and, hence, allowed for better detection of signals of adaptation via the microbiome. During the course of adaptation, we tested spider mite performance (number of eggs laid and longevity) and characterized the bacterial component of its microbiome (16S rRNA gene sequencing) to determine: (1) whether the bacterial communities were shaped by mite ancestry or plant environment and (2) whether the spider mites' performance and microbiome composition were related. We found that spider mite performance on the novel host plants was clearly correlated with microbiome composition. Because our results show that only little of the total variation in the microbiome can be explained by the properties of the host (spider mite) and the environment (plant species) we studied, we argue that the bacterial community within hosts could be valuable for understanding a species' performance on multiple resources.

The Demographic Consequences of Adaptation: Evidence from Experimental Evolution.

AbstractThe process of adaptation toward novel environments is directly connected to the acquisition of higher fitness relative to others. Such increased fitness is obtained by changes in life history traits that may directly impact population dynamics. From a functional perspective, increased fitness can be achieved through higher resource use or more efficient resource use, each potentially having its own impact on population dynamics. In the first case, adaptation is expected to directly translate into higher population growth. In the second case, adaptation requires less energy and hence may lead to higher carrying capacity. Adaptation may thus lead to changes in ecological dynamics and vice versa. Here, by using a combination of evolutionary experiments with spider mites and a population dynamic model, we investigate how an increase in fecundity (a validated proxy for adaptation) affects a population's ecological dynamics. Our results show that adaptation can positively affect population growth rate and either positively or negatively affect carrying capacity, depending on the ecological condition leading to variation in adaptation. These findings show the importance of evolution for population dynamics in changing environments, which may ultimately affect the stability and resilience of populations.

Contribution of opsins and chromophores to cone pigment variation across populations of Lake Victoria cichlids.

Adaptation to heterogeneous sensory environments has been implicated as a key parameter in speciation. Cichlid fish are a textbook example of divergent visual adaptation, mediated by variation in the sequences and expression levels of cone opsin genes (encoding the protein component of visual pigments). In some vertebrates including fish, visual sensitivity is also tuned by the ratio of vitamin A1 /A2 -derived chromophores (i.e., the light-sensitive component of the visual pigment bound to the opsin protein), where higher proportions of A2 cause a more red-shifted wavelength absorbance. This study explores the variation in chromophore ratios across multiple cichlid populations in Lake Victoria, using as a proxy the expression of the gene Cyp27c1, which has been shown to regulate the conversion of vitamin A1 into vitamin A2 in several vertebrates. This study focuses on sympatric Pundamilia cichlids, where species with blue or red male coloration co-occur at multiple islands but occupy different depths and consequently different visual habitats. In the red species, we found higher cyp27c1 expression in populations from turbid waters than from clear waters, but there was no such pattern in the blue species. Across populations, differences between the sympatric species in cyp27c1 expression had a consistent relationship with species differences in opsin expression patterns, but the red/blue identity reversed between clear and turbid waters. To assess the contribution of heritable vs. environmental causes of variation, we tested whether light manipulations induce a change in cyp27c1 expression in the laboratory. We found that cyp27c1 expression was not influenced by experimental light conditions, suggesting that the observed variation in the wild is due to genetic differences. Nonetheless, compared to other cichlid species, cyp27c1 is expressed at very low levels in Pundamilia, suggesting that it may not be relevant for visual adaptation in this species. Conclusively, establishing the biological importance of this variation requires testing of actual A1 /A2 ratios in the eye, as well as its consequences for visual performance.

Nucleotide Substitutions during Speciation may Explain Substitution Rate Variation.

Although molecular mechanisms associated with the generation of mutations are highly conserved across taxa, there is widespread variation in mutation rates between evolutionary lineages. When phylogenies are reconstructed based on nucleotide sequences, such variation is typically accounted for by the assumption of a relaxed molecular clock, which is a statistical distribution of mutation rates without much underlying biological mechanism. Here, we propose that variation in accumulated mutations may be partly explained by an elevated mutation rate during speciation. Using simulations, we show how shifting mutations from branches to speciation events impacts inference of branching times in phylogenetic reconstruction. Furthermore, the resulting nucleotide alignments are better described by a relaxed than by a strict molecular clock. Thus, elevated mutation rates during speciation potentially explain part of the variation in substitution rates that is observed across the tree of life. [Molecular clock; phylogenetic reconstruction; speciation; substitution rate variation.].

Miocene Climate and Habitat Change Drove Diversification in Bicyclus, Africa's Largest Radiation of Satyrine Butterflies.

Compared to other regions, the drivers of diversification in Africa are poorly understood. We studied a radiation of insects with over 100 species occurring in a wide range of habitats across the Afrotropics to investigate the fundamental evolutionary processes and geological events that generate and maintain patterns of species richness on the continent. By investigating the evolutionary history of Bicyclus butterflies within a phylogenetic framework, we inferred the group's origin at the Oligo-Miocene boundary from ancestors in the Congolian rainforests of central Africa. Abrupt climatic fluctuations during the Miocene (ca. 19-17 Ma) likely fragmented ancestral populations, resulting in at least eight early-divergent lineages. Only one of these lineages appears to have diversified during the drastic climate and biome changes of the early Miocene, radiating into the largest group of extant species. The other seven lineages diversified in forest ecosystems during the late Miocene and Pleistocene when climatic conditions were more favorable-warmer and wetter. Our results suggest changing Neogene climate, uplift of eastern African orogens, and biotic interactions have had different effects on the various subclades of Bicyclus, producing one of the most spectacular butterfly radiations in Africa. [Afrotropics; biodiversity; biome; biotic interactions; Court Jester; extinction; grasslands; paleoclimates; Red Queen; refugia forests; dependent-diversification; speciation.].

A unified model of species abundance, genetic diversity, and functional diversity reveals the mechanisms structuring ecological communities.

Biodiversity accumulates hierarchically by means of ecological and evolutionary processes and feedbacks. Within ecological communities drift, dispersal, speciation, and selection operate simultaneously to shape patterns of biodiversity. Reconciling the relative importance of these is hindered by current models and inference methods, which tend to focus on a subset of processes and their resulting predictions. Here we introduce massive ecoevolutionary synthesis simulations (MESS), a unified mechanistic model of community assembly, rooted in classic island biogeography theory, which makes temporally explicit joint predictions across three biodiversity data axes: (i) species richness and abundances, (ii) population genetic diversities, and (iii) trait variation in a phylogenetic context. Using simulations we demonstrate that each data axis captures information at different timescales, and that integrating these axes enables discriminating among previously unidentifiable community assembly models. MESS is unique in generating predictions of community-scale genetic diversity, and in characterizing joint patterns of genetic diversity, abundance, and trait values. MESS unlocks the full potential for investigation of biodiversity processes using multidimensional community data including a genetic component, such as might be produced by contemporary eDNA or metabarcoding studies. We combine MESS with supervised machine learning to fit the parameters of the model to real data and infer processes underlying how biodiversity accumulates, using communities of tropical trees, arthropods, and gastropods as case studies that span a range of data availability scenarios, and spatial and taxonomic scales.

Evolutionary dynamics of the elevational diversity gradient in passerine birds.

Low-elevation regions harbour the majority of the world's species diversity compared to high-elevation areas. This global gradient suggests that lowland species have had more time to diversify, or that net diversification rates have been higher in the lowlands. However, highlands seem to be cradles of diversity as they contain many young endemics, suggesting that their rates of speciation are exceptionally fast. Here we use a phylogenetic diversification model that accounts for the dispersal of species between different elevations to examine the evolutionary dynamics of the elevational diversity gradient in passerine birds, a group that has radiated globally to occupy almost all elevations and latitudes. We find strong support for a model in which passerines diversify at the same rate in the highlands and the lowlands but in which the per-capita rate of dispersal from high to low elevations is more than twice as fast as that in the reverse direction. This suggests that while there is no consistent trend in diversification across elevations, part of the diversity generated by highland regions migrates into the lowlands, thus setting up the observed gradient in passerine diversity. We find that this process drives tropical regions but for temperate areas, the analysis could be hampered by their lower richness. Despite their lower diversity, highland regions are disproportionally important for maintaining diversity in the adjacent lowlands.

Inferring the Effect of Species Interactions on Trait Evolution.

Models of trait evolution form an important part of macroevolutionary biology. The Brownian motion model and Ornstein-Uhlenbeck models have become classic (null) models of character evolution, in which species evolve independently. Recently, models incorporating species interactions have been developed, particularly involving competition where abiotic factors pull species toward an optimal trait value and competitive interactions drive the trait values apart. However, these models assume a fitness function rather than derive it from population dynamics and they do not consider dynamics of the trait variance. Here, we develop a general coherent trait evolution framework where the fitness function is based on a model of population dynamics, and therefore it can, in principle, accommodate any type of species interaction. We illustrate our framework with a model of abundance-dependent competitive interactions against a macroevolutionary background encoded in a phylogenetic tree. We develop an inference tool based on Approximate Bayesian Computation and test it on simulated data (of traits at the tips). We find that inference performs well when the diversity predicted by the parameters equals the number of species in the phylogeny. We then fit the model to empirical data of baleen whale body lengths, using three different summary statistics, and compare it to a model without population dynamics and a model where competition depends on the total metabolic rate of the competitors. We show that the unweighted model performs best for the least informative summary statistic, while the model with competition weighted by the total metabolic rate fits the data slightly better than the other two models for the two more informative summary statistics. Regardless of the summary statistic used, the three models substantially differ in their predictions of the abundance distribution. Therefore, data on abundance distributions will allow us to better distinguish the models from one another, and infer the nature of species interactions. Thus, our framework provides a conceptual approach to reveal species interactions underlying trait evolution and identifies the data needed to do so in practice. [Approximate Bayesian computation; competition; phylogeny; population dynamics; simulations; species interaction; trait evolution.].

Branching patterns in phylogenies cannot distinguish diversity-dependent diversification from time-dependent diversification.

One of the primary goals of macroevolutionary biology has been to explain general trends in long-term diversity patterns, including whether such patterns correspond to an upscaling of processes occurring at lower scales. Reconstructed phylogenies often show decelerated lineage accumulation over time. This pattern has often been interpreted as the result of diversity-dependent (DD) diversification, where the accumulation of species causes diversification to decrease through niche filling. However, other processes can also produce such a slowdown, including time dependence without diversity dependence. To test whether phylogenetic branching patterns can be used to distinguish these two mechanisms, we formulated a time-dependent, but diversity-independent model that matches the expected diversity through time of a DD model. We simulated phylogenies under each model and studied how well likelihood methods could recover the true diversification mode. Standard model selection criteria always recovered diversity dependence, even when it was not present. We correct for this bias by using a bootstrap method and find that neither model is decisively supported. This implies that the branching pattern of reconstructed trees contains insufficient information to detect the presence or absence of diversity dependence. We advocate that tests encompassing additional data, for example, traits or range distributions, are needed to evaluate how diversity drives macroevolutionary trends.

Microbiome and environment explain the absence of correlations between consumers and their diet in Bornean microsnails.

Classical ecological theory posits that species partition resources such that each species occupies a unique resource niche. In general, the availability of more resources allows more species to co-occur. Thus, a strong relationship between communities of consumers and their resources is expected. However, correlations may be influenced by other layers in the food web, or by the environment. Here we show, by studying the relationship between communities of consumers (land snails) and individual diets (from seed plants), that there is in fact no direct, or at most a weak but negative, relationship. However, we found that the diversity of the individual microbiome positively correlates with both consumer community diversity and individual diet diversity in three target species. Moreover, these correlations were affected by various environmental variables, such as anthropogenic activity, habitat island size, and a possibly important nutrient source, guano runoff from nearby caves. Our results suggest that the microbiome and the environment explain the absence of correlations between diet and consumer community diversity. Hence, we advocate that microbiome inventories are routinely added to any community dietary analysis, which our study shows can be done with relatively little extra effort. Our approach presents the tools to quickly obtain an overview of the relationships between consumers and their resources. We anticipate our approach to be useful for ecologists and environmentalists studying different communities in a local food web.

Detecting Lineage-Specific Shifts in Diversification: A Proper Likelihood Approach.

The branching patterns of molecular phylogenies are generally assumed to contain information on rates of the underlying speciation and extinction processes. Simple birth-death models with constant, time-varying, or diversity-dependent rates have been invoked to explain these patterns. They have one assumption in common: all lineages have the same set of diversification rates at a given point in time. It seems likely, however, that there is variability in diversification rates across subclades in a phylogenetic tree. This has inspired the construction of models that allow multiple rate regimes across the phylogeny, with instantaneous shifts between these regimes. Several methods exist for calculating the likelihood of a phylogeny under a specified mapping of diversification regimes and for performing inference on the most likely diversification history that gave rise to a particular phylogenetic tree. Here, we show that the likelihood computation of these methods is not correct. We provide a new framework to compute the likelihood correctly and show, with simulations of a single shift, that the correct likelihood indeed leads to parameter estimates that are on average in much better agreement with the generating parameters than the incorrect likelihood. Moreover, we show that our corrected likelihood can be extended to multiple rate shifts in time-dependent and diversity-dependent models. We argue that identifying shifts in diversification rates is a nontrivial model selection exercise where one has to choose whether shifts in now-extinct lineages are taken into account or not. Hence, our framework also resolves the recent debate on such unobserved shifts. [Diversification; macroevolution; phylogeny; speciation].

Performance in a novel environment subject to ghost competition.

BACKGROUND: A central tenet of the evolutionary theory of communities is that competition impacts evolutionary processes such as local adaptation. Species in a community exert a selection pressure on other species and may drive them to extinction. We know, however, very little about the influence of unsuccessful or ghost species on the evolutionary dynamics within the community. METHODS: Here we report the long-term influence of a ghost competitor on the performance of a more successful species using experimental evolution. We transferred the spider mite Tetranychus urticae onto a novel host plant under initial presence or absence of a competing species, the congeneric mite T. ludeni. RESULTS: The competitor species, T. ludeni, unintentionally went extinct soon after the start of the experiment, but we nevertheless completed the experiment and found that the early competitive pressure of this ghost competitor positively affected the performance (i.e., fecundity) of the surviving species, T. urticae. This effect on T. urticae lasted for at least 25 generations. DISCUSSION: Our study suggests that early experienced selection pressures can exert a persistent evolutionary signal on species' performance in novel environments.

A simple dynamic model explains the diversity of island birds worldwide.

Colonization, speciation and extinction are dynamic processes that influence global patterns of species richness1-6. Island biogeography theory predicts that the contribution of these processes to the accumulation of species diversity depends on the area and isolation of the island7,8. Notably, there has been no robust global test of this prediction for islands where speciation cannot be ignored9, because neither the appropriate data nor the analytical tools have been available. Here we address both deficiencies to reveal, for island birds, the empirical shape of the general relationships that determine how colonization, extinction and speciation rates co-vary with the area and isolation of islands. We compiled a global molecular phylogenetic dataset of birds on islands, based on the terrestrial avifaunas of 41 oceanic archipelagos worldwide (including 596 avian taxa), and applied a new analysis method to estimate the sensitivity of island-specific rates of colonization, speciation and extinction to island features (area and isolation). Our model predicts-with high explanatory power-several global relationships. We found a decline in colonization with isolation, a decline in extinction with area and an increase in speciation with area and isolation. Combining the theoretical foundations of island biogeography7,8 with the temporal information contained in molecular phylogenies10 proves a powerful approach to reveal the fundamental relationships that govern variation in biodiversity across the planet.

Additional Analytical Support for a New Method to Compute the Likelihood of Diversification Models.

Molecular phylogenies have been increasingly recognized as an important source of information on species diversification. For many models of macroevolution, analytical likelihood formulas have been derived to infer macroevolutionary parameters from phylogenies. A few years ago, a general framework to numerically compute such likelihood formulas was proposed, which accommodates models that allow speciation and/or extinction rates to depend on diversity. This framework calculates the likelihood as the probability of the diversification process being consistent with the phylogeny from the root to the tips. However, while some readers found the framework presented in Etienne et al. (Proc R Soc Lond B Biol Sci 279(1732):1300-1309, 2012) convincing, others still questioned it (personal communication), despite numerical evidence that for special cases the framework yields the same (i.e., within double precision) numerical value for the likelihood as analytical formulas do that were independently derived for these special cases. Here we prove analytically that the likelihoods calculated in the new framework are correct for all special cases with known analytical likelihood formula. Our results thus add substantial mathematical support for the overall coherence of the general framework.

A Minimal Model for the Latitudinal Diversity Gradient Suggests a Dominant Role for Ecological Limits.

The latitudinal diversity gradient (LDG) is one of Earth's most iconic biodiversity patterns and still one of the most debated. Explanations for the LDG are often categorized into three broad pathways in which the diversity gradient is created by (1) differential diversification rates, (2) differential carrying capacities (ecological limits), or (3) differential time to accumulate species across latitude. Support for these pathways has, however, been mostly verbally expressed. Here, we present a minimal model to clarify the essential assumptions of the three pathways and explore the sensitivity of diversity dynamics to these pathways. We find that an LDG arises most easily from a gradient in ecological limits compared with a gradient in the time for species accumulation or diversification rate in most modeled scenarios. Differential diversification rates create a stronger LDG than ecological limits only when speciation and dispersal rates are low, but then the predicted LDG seems weaker than the observed LDG. Moreover, range dynamics may reduce an LDG created by a gradient in diversification rates or time for species accumulation, but they cannot reduce an LDG induced by differential ecological limits. We conclude that our simple model provides a null prediction for the effectiveness of the three LDG pathways and can thus aid discussions about the causal mechanisms underlying the LDG or motivate more complex models to confirm or falsify our findings.