Mating patterns influence vulnerability to the extinction vortex

Earth's biodiversity is undergoing mass extinction due to anthropogenic compounding of environmental, demographic and genetic stresses. These different stresses can trap populations within a reinforcing feedback loop known as the extinction vortex, in which synergistic pressures build upon one another through time, driving down population viability. Sexual selection, the widespread evolutionary force arising from competition, choice and reproductive variance within animal mating patterns could have vital consequences for population viability and the extinction vortex: (a) if sexual selection reinforces natural selection to fix ‘good genes’ and purge ‘bad genes’, then mating patterns encouraging competition and choice may help protect populations from extinction; (b) by contrast, if mating patterns create load through evolutionary or ecological conflict, then population viability could be further reduced by sexual selection. We test between these opposing theories using replicate populations of the model insect Tribolium castaneum exposed to over 10 years of experimental evolution under monogamous versus polyandrous mating patterns. After a 95‐generation history of divergence in sexual selection, we compared fitness and extinction of monogamous versus polyandrous populations through an experimental extinction vortex comprising 15 generations of cycling environmental and genetic stresses. Results showed that lineages from monogamous evolutionary backgrounds, with limited opportunities for sexual selection, showed rapid declines in fitness and complete extinction through the vortex. By contrast, fitness of populations from the history of polyandry, with stronger opportunities for sexual selection, declined slowly, with 60% of populations surviving by the study end. The three vortex stresses of (a) nutritional deprivation, (b) thermal stress and (c) genetic bottlenecking had similar impacts on fitness declines and extinction risk, with an overall sigmoid decline in survival through time. We therefore reveal sexual selection as an important force behind lineages facing extinction threats, identifying the relevance of natural mating patterns for conservation management.     

Biological hierarchies and the nature of extinction

Hierarchy theory recognises that ecological and evolutionary units occur in a nested and interconnected hierarchical system, with cascading effects occurring between hierarchical levels. Different biological disciplines have routinely come into conflict over the primacy of different forcing mechanisms behind evolutionary and ecological change. These disconnects arise partly from differences in perspective (with some researchers favouring ecological forcing mechanisms while others favour developmental/historical mechanisms), as well as differences in the temporal framework in which workers operate. In particular, long‐term palaeontological data often show that large‐scale (macro) patterns of evolution are predominantly dictated by shifts in the abiotic environment, while short‐term (micro) modern biological studies stress the importance of biotic interactions. We propose that thinking about ecological and evolutionary interactions in a hierarchical framework is a fruitful way to resolve these conflicts. Hierarchy theory suggests that changes occurring at lower hierarchical levels can have unexpected, complex effects at higher scales due to emergent interactions between simple systems. In this way, patterns occurring on short‐ and long‐term time scales are equally valid, as changes that are driven from lower levels will manifest in different forms at higher levels. We propose that the dual hierarchy framework fits well with our current understanding of evolutionary and ecological theory. Furthermore, we describe how this framework can be used to understand major extinction events better. Multi‐generational attritional loss of reproductive fitness (MALF) has recently been proposed as the primary mechanism behind extinction events, whereby extinction is explainable solely through processes that result in extirpation of populations through a shutdown of reproduction. While not necessarily explicit, the push to explain extinction through solely population‐level dynamics could be used to suggest that environmentally mediated patterns of extinction or slowed speciation across geological time are largely artefacts of poor preservation or a coarse temporal scale. We demonstrate how MALF fits into a hierarchical framework, showing that MALF can be a primary forcing mechanism at lower scales that still results in differential survivorship patterns at the species and clade level which vary depending upon the initial environmental forcing mechanism. Thus, even if MALF is the primary mechanism of extinction across all mass extinction events, the primary environmental cause of these events will still affect the system and result in differential responses. Therefore, patterns at both temporal scales are relevant.     

Macroecology and the hierarchical expansion of evolutionary theory

The constraint envelope describing the relationship between geographical range size and body size has usually been explained by a minimum viable population size model, furnishing a strong argument for species selection if geographical range size turns out to be ‘heritable’. Recent papers have questioned this assumption of nonzero geographical range heritability at a phylogenetic level, meaning that the logic that constraint envelopes provide support for higher‐level selection fails. However, I believe that analysis of constraint envelopes can still furnish insights for the hierarchical expansion of evolutionary theory because the fitness furnished by variation in body size, which is frequently measured as a highly ‘heritable’ trait at the species level, can be partitioned into anagenetic and cladogenetic components. The constraint envelope furnishes an explicit mechanism for large‐body biased extinction rates influencing the distribution of body size. More importantly, it is possible to envisage a scenario in which anagenetic trends driving an increase in body size in higher latitudes within species (Bergmann's rule) are counteracted by available habitat area or continental edges constraining overall species distribution in these higher latitudes, increasing the probability of extinction. Under this combined model, faunas at higher latitudes and under habitat constraints may reach equilibrium points between these opposing hierarchical adaptive forces at smaller body size than faunas with less intense higher‐level constraints and will tend to be more right‐skewed.     

An evolutionary tipping point in a changing environment

Populations can persist in directionally changing environments by evolving. Quantitative genetic theory aims to predict critical rates of environmental change beyond which populations go extinct. Here, we point out that all current predictions effectively assume the same specific fitness function. This function causes selection on the standing genetic variance of quantitative traits to become increasingly strong as mean trait values depart from their optima. Hence, there is no bound on the rate of evolution and persistence is determined by the critical rate of environmental change at which populations cease to grow. We then show that biologically reasonable changes to the underlying fitness function can impose a qualitatively different extinction threshold. In particular, inflection points caused by weakening selection create local extrema in the strength of selection and thus in the rate of evolution. These extrema can produce evolutionary tipping points, where long‐run population growth rates drop from positive to negative values without ever crossing zero. Generic early‐warning signs of tipping points are found to have little power to detect imminent extinction, and require hard‐to‐gather data. Furthermore, we show how evolutionary tipping points produce evolutionary hysteresis, creating extinction debts.     

Predicting patterns of long‐term adaptation and extinction with population genetics

Population genetics struggles to model extinction; standard models track the relative rather than absolute fitness of genotypes, while the exceptions describe only the short‐term transition from imminent doom to evolutionary rescue. But extinction can result from failure to adapt not only to catastrophes, but also to a backlog of environmental challenges. We model long‐term adaptation to long series of small challenges, where fitter populations reach higher population sizes. The population's long‐term fitness dynamic is well approximated by a simple stochastic Markov chain model. Long‐term persistence occurs when the rate of adaptation exceeds the rate of environmental deterioration for some genotypes. Long‐term persistence times are consistent with typical fossil species persistence times of several million years. Immediately preceding extinction, fitness declines rapidly, appearing as though a catastrophe disrupted a stably established population, even though gradual evolutionary processes are responsible. New populations go through an establishment phase where, despite being demographically viable, their extinction risk is elevated. Should the population survive long enough, extinction risk later becomes constant over time.     

Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection

Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree‐derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so‐called “paradox of stasis.” To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies—which have largely been limited to birds and mammals—to study evolutionary processes on contemporary timescales.     

SCALE AND HIERARCHY IN MACROEVOLUTION

Abstract: Scale and hierarchy must be incorporated into any conceptual framework for the study of macroevolution, i.e. evolution above the species level. Expansion of temporal and spatial scales reveals evolutionary patterns and processes that are virtually inaccessible to, and unpredictable from, short‐term, localized observations. These larger‐scale phenomena range from evolutionary stasis at the species level and the mosaic assembly of complex morphologies in ancestral forms to the non‐random distribution in time and space of the origin of major evolutionary novelties, as exemplified by the Cambrian explosion and post‐extinction recoveries of metazoans, and the preferential origin of major marine groups in onshore environments and tropical waters. Virtually all of these phenomena probably involve both ecological and developmental factors, but the integration of these components with macroevolutionary theory has only just begun. Differential survival and reproduction of units can occur at several levels within a biological hierarchy that includes DNA sequences, organisms, species and clades. Evolution by natural selection can occur at any level where there is heritable variation that affects birth and death of units by virtue of interaction with the environment. This dynamic can occur when selfish DNA sequences replicate disproportionately within genomes, when organisms enjoy fitness advantages within populations (classical Darwinian selection), when differential speciation or extinction occurs within clades owing to organismic properties (effect macroevolution), and when differential speciation or extinction occurs within clades owing to emergent, species‐level properties (in the strict sense species selection). Operationally, emergent species‐level properties such as geographical range can be recognized by testing whether their macroevolutionary effects are similar regardless of the different lower‐level factors that produce them. Large‐scale evolutionary trends can be driven by transformation of species, preferential production of species in a given direction, differential origination or extinction, or any combination of these; the potential for organismic traits to hitch‐hike on other factors that promote speciation or damp extinction is high. Additional key attributes of macroevolutionary dynamics within biological hierarchies are that (1) hierarchical levels are linked by upward and downward causation, so that emergent properties at a focal level do not impart complete independence; (2) hierarchical effects are asymmetrical, so that dynamics at a given focal level need not propagate upwards, but will always cascade downwards; and (3) rates are generally, although not always, faster at lower hierarchical levels. Temporal and spatial patterns in the origin of major novelties and higher taxa are significantly discordant from those at the species and genus levels, suggesting complex hierarchical effects that remain poorly understood. Not only are many of the features promoting survivorship during background times ineffective during mass extinctions, but also they are replaced in at least some cases by higher‐level, irreducible attributes such as clade‐level geographical range. The incorporation of processes that operate across hierarchical levels and a range of temporal and spatial scales has expanded and enriched our understanding of evolution.     

Genetic and environmental effects on a condition‐dependent trait: feather growth in Siberian jays

Condition, defined as the amount of ‘internal resources’ an individual can freely allocate, is often assumed to be environmentally determined and to reflect an individual’s health and nutritional status. However, an additive genetic component of condition is possible if it ‘captures’ the genetic variance of many underlying traits as many fitness‐related traits appear to do. Yet, the heritability of condition can be low if selection has eroded much of its additive genetic variance, or if the environmental influences are strong. Here, we tested whether feather growth rate – presumably a condition‐dependent trait – has a heritable component, and whether variation in feather growth rate is related to variation in fitness. To this end, we utilized data from a long‐term population study of Siberian jays (Perisoreus infaustus), and found that feather growth rate, measured as the width of feather growth bars (GB), differed between age‐classes and sexes, but was only weakly related to variation in fitness as measured by annual and life‐time reproductive success. As revealed by animal model analyses, GB width was significantly heritable (h² = 0.10 ± 0.05), showing that this measure of condition is not solely environmentally determined, but reflects at least partly inherited genetic differences among individuals. Consequently, variation in feather growth rates as assessed with ptilochronological methods can provide information about heritable genetic differences in condition.     

Exploring the phylogenetic history of mammal species richness

Aim At broad geographical scales, species richness is a product of three basic processes: speciation, extinction and migration. However, determining which of these processes predominates is a major challenge. Whilst palaeontological studies can provide information on speciation and extinction rates, data are frequently lacking. Here we use a recent dated phylogenetic tree of mammals to explore the relative importance of these three processes in structuring present‐day richness gradients. Location The global terrestrial biosphere. Methods We combine macroecological data with phylogenetic methods more typically used in community ecology to describe the phylogenetic history of regional faunas. Using simulations, we explore two simple phylogenetic metrics, the mean and variance in the pairwise distances between taxa, and describe their relationship to phylogenetic tree topology. We then use these two metrics to characterize the evolutionary relationships among mammal species assemblages across the terrestrial biome. Results We show that the mean and variance in the pairwise distances describe phylogenetic tree topology well, but are less sensitive to phylogenetic uncertainty than more direct measures of tree shape. We find the phylogeny for South American mammals is imbalanced and ‘stemmy’ (long branches towards the root), consistent with recent diversification within evolutionarily disparate lineages. In contrast, the phylogeny for African mammals is balanced and ‘tippy’ (long branches towards the tips), more consistent with the slow accumulation of diversity over long times, reflecting the Old World origin of many mammal clades. Main conclusions We show that phylogeny can accurately capture biogeographical processes operating at broad spatial scales and over long time periods. Our results support inferences from the fossil record – that the New World tropics are a diversity cradle whereas the Old World tropics are a museum of old diversity.     

Evolutionary regime shifts in simulated ecosystems

Catastrophic regime shifts in ecosystems occur when the system is tipped into a new attractor state under some external forcing. Here we consider whether evolutionary adaptations within ecosystems can trigger similar transitions. We use an individual‐based, evolutionary model of interconnected ecosystems to analyze nonlinear changes in global state resulting from local adaptations. Transitions between periods of stability occur when new traits arise that allow exploitation of under‐utilized resources. Subsequent rapid growth of the population carrying the new trait causes abrupt environmental change that drives incumbent species extinct. We call these transitions ‘evolutionary regime shifts’. These internally generated perturbations can result in ecosystem collapse, followed by recovery to an alternate stable state, or occasionally system‐wide extinction. While these disruptions may have a negative impact on ecosystem productivity in individual simulation runs, mean results over many simulations show a trend for increasing ecosystem productivity and stability over time. Feedback between life and the abiotic environment in the model creates a ‘long‐tailed’ distribution of extinction sizes without any external trigger for large extinction events.     

Predicting evolutionary potential: A numerical test of evolvability measures

Despite sophisticated mathematical models, the theory of microevolution is mostly treated as a qualitative rather than a quantitative tool. Numerical measures of selection, constraints, and evolutionary potential are often too loosely connected to theory to provide operational predictions of the response to selection. In this paper, we study the ability of a set of operational measures of evolvability and constraint to predict short‐term selection responses generated by individual‐based simulations. We focus on the effects of selective constraints under which the response in one trait is impeded by stabilizing selection on other traits. The conditional evolvability is a measure of evolutionary potential explicitly developed for this situation. We show that the conditional evolvability successfully predicts rates of evolution in an equilibrium situation, and further that these equilibria are reached with characteristic times that are inversely proportional to the fitness load generated by the constraining characters. Overall, we find that evolvabilities and conditional evolvabilities bracket responses to selection, and that they together can be used to quantify evolutionary potential on time scales where the G‐matrix remains relatively constant.     

The pace of modern life II: from rates of contemporary microevolution to pattern and process

We compiled a database of microevolution on contemporary time scales in nature (47 source articles; 30 animal species), comprising 2649 evolutionary rates in darwins (proportional change per million years) and 2151 evolutionary rates in haldanes (standard deviations per generation). Here we demonstrate how quantitative rate measures can provide general insights into patterns and processes of evolution. The frequency distribution of evolutionary rates was approximately log-normal, with many slow rates and few fast rates. Net selection intensities estimated from haldanes were on average lower than selection intensities commonly measured directly in natural populations. This difference suggests that natural selection could easily accomplish observed microevolution but that the intensities of selection typically measured in nature are rarely maintained for long (otherwise observed evolutionary rates would be higher). Traits closely associated with fitness (life history traits) appear to evolve at least as fast as traits less closely tied to fitness (morphology). The magnitude of evolutionary difference increased with the length of the time interval, particularly when maximum rates from a given study were considered. This pattern suggests a general underlying tendency toward increasing evolutionary diversification with time. However, evolutionary rates also tended to decrease with time, perhaps because longer time intervals average increasingly disparate rates over time, or because evolution slows when populations approach new optima or as genetic variation is depleted. In combination, our results suggest that macroevolutionary transitions may ultimately arise through microevolution occasionally writ large but are perhaps temporally characterized by microevolution writ in fits and starts.     

Life‐history evolution under fluctuating density‐dependent selection and the adaptive alignment of pace‐of‐life syndromes

We present a novel perspective on life‐history evolution that combines recent theoretical advances in fluctuating density‐dependent selection with the notion of pace‐of‐life syndromes (POLSs) in behavioural ecology. These ideas posit phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits as a continuum from the highly fecund, short‐lived, bold, aggressive and highly dispersive ‘fast’ types at one end of the POLS to the less fecund, long‐lived, cautious, shy, plastic and socially responsive ‘slow’ types at the other. We propose that such variation in life histories and the associated individual differences in behaviour can be explained through their eco‐evolutionary dynamics with population density – a single and ubiquitous selective factor that is present in all biological systems. Contrasting regimes of environmental stochasticity are expected to affect population density in time and space and create differing patterns of fluctuating density‐dependent selection, which generates variation in fast versus slow life histories within and among populations. We therefore predict that a major axis of phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits (i.e. the POLS) should align with these stochastic fluctuations in the multivariate fitness landscape created by variation in density‐dependent selection. Phenotypic plasticity and/or genetic (co‐)variation oriented along this major POLS axis are thus expected to facilitate rapid and adaptively integrated changes in various aspects of life histories within and among populations and/or species. The fluctuating density‐dependent selection POLS framework presented here therefore provides a series of clear testable predictions, the investigation of which should further our fundamental understanding of life‐history evolution and thus our ability to predict natural population dynamics.     

Surfing on the seascape: Adaptation in a changing environment

The environment changes constantly at various time scales and, in order to survive, species need to keep adapting. Whether these species succeed in avoiding extinction is a major evolutionary question. Using a multilocus evolutionary model of a mutation‐limited population adapting under strong selection, we investigate the effects of the frequency of environmental fluctuations on adaptation. Our results rely on an “adaptive‐walk” approximation and use mathematical methods from evolutionary computation theory to investigate the interplay between fluctuation frequency, the similarity of environments, and the number of loci contributing to adaptation. First, we assume a linear additive fitness function, but later generalize our results to include several types of epistasis. We show that frequent environmental changes prevent populations from reaching a fitness peak, but they may also prevent the large fitness loss that occurs after a single environmental change. Thus, the population can survive, although not thrive, in a wide range of conditions. Furthermore, we show that in a frequently changing environment, the similarity of threats that a population faces affects the level of adaptation that it is able to achieve. We check and supplement our analytical results with simulations.     

The mechanism of background extinction

Following publication of On the Origin of Species, biologists concentrated on and resolved the mechanisms of adaptation and speciation, but largely ignored extinction. Thus, extinction remained essentially a discipline of palaeontology. Adequate language is not available to describe extinction phenomena because they must be discussed in the passive voice, wherein populations simply ‘go extinct’ without reference to process, specifics, effects, or causality. Extinction is also described typically in terms of its dynamics (including rate or risk), and although correlative variables enhance our ability to predict extinction, they do not necessarily enable an understanding of process. Yet background extinction, like evolution, is a process requiring a functional explanation, without which it is impossible to formulate mechanisms. We define the mechanism of background extinction as a typically long‐term, multi‐generational loss of reproductive fitness. This simple concept has received little credence because of a perception that excess generation of progeny ensures population sustainability, and perhaps the misconception that the loss of reproductive fitness somehow constitutes selection against reproduction itself. During environmental shifts, reproductive fitness is compromised when biotic or abiotic extremes consistently exceed existing norms of reaction. Subsequent selection will now favour individual survival over reproductive fitness, initiating long‐term negative selection pressure and population decline. Background extinction consists typically of two intergrading phases: habitat attenuation and habitat dissolution. These processes generate the relict populations that characterize many species undergoing background extinction. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 255–268.     

Taming fitness: Organism‐environment interdependencies preclude long‐term fitness forecasting

Fitness is a central but notoriously vexing concept in evolutionary biology. The propensity interpretation of fitness is often regarded as the least problematic account for fitness. It ties an individual's fitness to a probabilistic capacity to produce offspring. Fitness has a clear causal role in evolutionary dynamics under this account. Nevertheless, the propensity interpretation faces its share of problems. We discuss three of these. We first show that a single scalar value is an incomplete summary of a propensity. Second, we argue that the widespread method of “abstracting away” environmental idiosyncrasies by averaging over reproductive output in different environments is not a valid approach when environmental changes are irreversible. Third, we point out that expanding the range of applicability for fitness measures by averaging over more environments or longer time scales (so as to ensure environmental reversibility) reduces one's ability to distinguish selectively relevant differences among individuals because of mutation and eco‐evolutionary feedbacks. This series of problems leads us to conclude that a general value of fitness that is both explanatory and predictive cannot be attained. We advocate for the use of propensity‐compatible methods, such as adaptive dynamics, which can accommodate these difficulties.     

Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation

Xiphosurids are an archaic group of aquatic chelicerate arthropods, generally known by the colloquial misnomer of ‘horseshoe crabs’. Known from marine environments as far back as the early Ordovician, horseshoe crabs are generally considered ‘living fossils’ – descendants of a bradytelic lineage exhibiting little morphological or ecological variation throughout geological time. However, xiphosurids are known from freshwater sediments in the Palaeozoic and Mesozoic; furthermore, the contention that xiphosurids show little morphological variation has never been tested empirically. Attempts to test this are hampered by the lack of a modern phylogenetic framework with which to explore different evolutionary scenarios. Here, I present a phylogenetic analysis of Xiphosurida and explore patterns of morphospace and environmental occupation of the group throughout the Phanerozoic. Xiphosurids are shown to have invaded non‐marine environments independently at least five times throughout their evolutionary history, twice resulting in the radiation of major clades – bellinurines and austrolimulids – that occupied novel regions of morphospace. These clades show a convergent ecological pattern of differentiation, speciation and subsequent extinction. Horseshoe crabs are shown to have a more dynamic and complex evolutionary history than previously supposed, with the extant species representing only a fraction of the group's past ecological and morphological diversity.     

Integrating over uncertainty in spatial scale of response within multispecies occupancy models yields more accurate assessments of community composition

Species abundance and community composition are affected not only by the local environment, but also by broader landscape and regional context. Yet, determining the spatial scales at which landscapes affect species remains a persistent challenge, hindering our ability to understand how environmental gradients shape communities. This problem is amplified by rare species and imperfect species detection. Here, we present a Bayesian framework that allows uncertainty surrounding the ‘true’ spatial scale of species’ responses (i.e. changes in presence/absence) to be integrated directly into a community hierarchical model. This scale‐selecting multispecies occupancy model (ssMSOM) estimates the scale of response, and shows high accuracy and correct levels of uncertainty in parameter estimates across a broad range of simulation conditions. An ssMSOM can be run in a matter of minutes, as opposed to the many hours required to run normal multispecies occupancy models at all queried spatial scales, and then conduct model selection – a problem that up to now has prohibited scale of response from being rigorously evaluated in an occupancy framework. Alternatives to the ssMSOM, such as GLM‐based approaches frequently fail to detect the correct spatial scale and magnitude of response, and are often falsely confident by favoring the incorrect parameter estimates, especially as species’ detection probabilities deviate from perfect. We further show how trait information can be leveraged to understand how individual species’ scales of response vary within communities. Integrating spatial scale selection directly into hierarchical community models provides a means of formally testing hypotheses regarding spatial scales of response, and more accurately determining the environmental drivers that shape communities.     

Reproductive failure: a new paradigm for extinction

Extinction was recognized as a scientific fact 200 years ago, although no adequate paradigm has emerged to explain the process. Prevailing theory has focused on ‘cause(s)’ of extinction but has neglected ‘effect’ and ‘mechanism’. These omissions preclude the formulation of a functional paradigm necessary for remedial action in response to the impending anthropogenic mediated, worldwide extinction crisis. The new paradigm is defined as the multi‐generational, attritional loss of reproductive fitness. Stabilizing selection continuously adapts species to specific ecosystems, which often results in highly evolved species prone to extinction when environments shift. Some species survive by tracking the declining palaeoclimates in which they presumably evolved, often becoming relicts prior to extinction. Compelling new evidence shows that even mass extinctions are largely a result of environmental change leading to widespread, attritional reproductive decline, rather than a result of instantaneous global catastrophes.