Rates Of Phenotypic Change Research Articles

A multiple variance Brownian motion framework for estimating variable rates and inferring ancestral states

To understand the nature of the evolutionary process, it is of paramount importance that temporal patterns of change in biological traits are accurately documented. The paleontological record is, however, inherently incomplete, leaving researchers with only a limited set of observed taxonomic units (OTUs) to estimate broader patterns of biological change. In this context, phylogenetic comparative methods have been developed aiming to estimate patterns of phenotypic change through time based on a phylogenetic tree and a limited set of OTUs. Such methods typically employ mathematical models proposing how change is likely to have unfolded over time. The most commonly used model, Brownian motion (BM), assumes that average trait change is proportional to the square root of time and that the rate of evolution is stochastically constant across all branches. This, however, lies in contrast to the commonly agreed notion that many biological traits change at different rates along different branches of the tree of life. We present a method for inferring ancestral states that allows for different evolutionary rates along different branches of the phylogenetic tree. The goal is to include the effects of variation in rates of phenotypic change across phylogenetic space. Based on the available phenotypic and phylogenetic information, we estimate measures of the rate of evolution on each individual branch and, subsequently, these estimates are used to parameterize a multiple variance BM model inferring the phenotypic values at all internal nodes. We demonstrate the validity of our approach with a series of simulations and an empirical example. We show that values for internal nodes inferred using our approach are equivalent to those inferred with a constant variance BM model if phenotypic evolution occurs according to standard BM. When evolution occurs at different rates along different branches of the phylogeny, our approach greatly outperforms constant variance BM. We further demonstrate that our approach accurately detects bursts of change in phylogenetic space. An empirical analysis of the evolution of primate brain and body mass reveals that our approach yields an improved statistical fit relative to both traditional and recent methods, and provides estimates of nodal values that lie within a range expected based on the fossil record.

How fast is fast? Eco-evolutionary dynamics and rates of change in populations and phenotypes.

It is increasingly recognized that evolution may occur in ecological time. It is not clear, however, how fast evolution - or phenotypic change more generally - may be in comparison with the associated ecology, or whether systems with fast ecological dynamics generally have relatively fast rates of phenotypic change. We developed a new dataset on standardized rates of change in population size and phenotypic traits for a wide range of species and taxonomic groups. We show that rates of change in phenotypes are generally no more than 2/3, and on average about 1/4, the concurrent rates of change in population size. There was no relationship between rates of population change and rates of phenotypic change across systems. We also found that the variance of both phenotypic and ecological rates increased with the mean across studies following a power law with an exponent of two, while temporal variation in phenotypic rates was lower than in ecological rates. Our results are consistent with the view that ecology and evolution may occur at similar time scales, but clarify that only rarely do populations change as fast in traits as they do in abundance.

Effects of pathogen exposure on life-history variation in the gypsymoth (Lymantria dispar).

Investment in host defences against pathogens may lead to trade-offs with host fecundity. When such trade-offs arise from genetic correlations, rates of phenotypic change by natural selection may be affected. However, genetic correlations between host survival and fecundity are rarely quantified. To understand trade-offs between immune responses to baculovirus exposure and fecundity in the gypsy moth (Lymantria dispar), we estimated genetic correlations between survival probability and traits related to fecundity, such as pupal weight. In addition, we tested whether different virus isolates have different effects on male and female pupal weight. To estimate genetic correlations, we exposed individuals of known relatedness to a single baculovirus isolate. To then evaluate the effect of virus isolate on pupal weight, we exposed a single gypsy moth strain to 16 baculovirus isolates. We found a negative genetic correlation between survival and pupal weight. In addition, virus exposure caused late-pupating females to be identical in weight to males, whereas unexposed females were 2-3 times as large as unexposed males. Finally, we found that female pupal weight is a quadratic function of host mortality across virus isolates, which is likely due to trade-offs and compensatory growth processes acting at high and low mortality levels, respectively. Overall, our results suggest that fecundity costs may strongly affect the response to selection for disease resistance. In nature, baculoviruses contribute to the regulation of gypsy moth outbreaks, as pathogens often do in forest-defoliating insects. We therefore argue that trade-offs between host life-history traits may help explain outbreak dynamics.

Linking macrotrends and microrates: Re-evaluating microevolutionary support for Cope's rule.

Cope's rule, wherein a lineage increases in body size through time, was originally motivated by macroevolutionary patterns observed in the fossil record. More recently, some authors have argued that evidence exists for generally positive selection on individual body size in contemporary populations, providing a microevolutionary mechanism for Cope's rule. If larger body size confers individual fitness advantages as the selection estimates suggest, thereby explaining Cope's rule, then body size should increase over microevolutionary time scales. We test this corollary by assembling a large database of studies reporting changes in phenotypic body size through time in contemporary populations, as well as studies reporting average breeding values for body size through time. Trends in body size were quite variable with an absence of any general trend, and many populations trended toward smaller body sizes. Although selection estimates can be interpreted to support Cope's rule, our results suggest that actual rates of phenotypic change for body size cannot. We discuss potential reasons for this discrepancy and its implications for the understanding of Cope's rule.

Effects of epistasis on infectivity range during host-parasite coevolution.

Understanding how parasites adapt to changes in host resistance is crucial to evolutionary epidemiology. Experimental studies have demonstrated that parasites are more capable of adapting to gradual, rather than sudden changes in host phenotype, as the latter may require multiple mutations that are unlikely to arise simultaneously. A key, but as yet unexplored factor is precisely how interactions between mutations (epistasis) affect parasite evolution. Here, we investigate this phenomenon in the context of infectivity range, where parasites may experience selection to infect broader sets of genotypes. When epistasis is strongly positive, we find that parasites are unlikely to evolve broader infectivity ranges if hosts exhibit sudden, rather than gradual changes in phenotype, in close agreement with empirical observations. This is due to a low probability of fixing multiple mutations that individually confer no immediate advantage. When epistasis is weaker, parasites are more likely to evolve broader infectivity ranges if hosts make sudden changes in phenotype, which can be explained by a balance between mutation supply and selection. Thus, we demonstrate that both the rate of phenotypic change in hosts and the form of epistasis between mutations in parasites are crucial in shaping the evolution of infectivity range.

How fast is fisheries‐induced evolution? Quantitative analysis of modelling and empirical studies

A number of theoretical models, experimental studies and time-series studies of wild fish have explored the presence and magnitude of fisheries-induced evolution (FIE). While most studies agree that FIE is likely to be happening in many fished stocks, there are disagreements about its rates and implications for stock viability. To address these disagreements in a quantitative manner, we conducted a meta-analysis of FIE rates reported in theoretical and empirical studies. We discovered that rates of phenotypic change observed in wild fish are about four times higher than the evolutionary rates reported in modelling studies, but correlation between the rate of change and instantaneous fishing mortality (F) was very similar in the two types of studies. Mixed-model analyses showed that in the modelling studies traits associated with reproductive investment and growth evolved slower than rates related to maturation. In empirical observations age-at-maturation was changing faster than other life-history traits. We also found that, despite different assumption and modelling approaches, rates of evolution for a given F value reported in 10 of 13 modelling studies were not significantly different.

History, haldanes and health inequities: exploring phenotypic changes in body size by generation and income level in the US-born White and Black non-Hispanic populations 1959-1962 to 2005-2008

Most public health literature on trends in population health and health inequities pertains to observed or targeted changes in rates or proportions per year or decade. We explore, in novel analyses, whether additional insight can be gained by using the 'haldane', a metric developed by evolutionary biologists to measure change in traits in standard deviations per generation, thereby enabling meaningful comparisons across species and time periods. We analysed the phenotypic embodied traits of body height, weight and body mass index of US-born White and Black non-Hispanic adults ages 20 to 44 as measured in six large nationally representative population samples spanning from the 1959-1962 National Health Examination Survey I to the 2005-2008 National Health and Nutrition Examination Survey. Setting the former as baseline, we computed the haldane for each outcome for each racial/ethnic group for each survey, overall and stratified by family income quintile. For height, high rates of phenotypic change (haldane ≥ 0.3) occurred chiefly between 1960 and 1980, especially for the Black population in the higher income quintiles. By contrast, for weight, high rates of phenotypic change became evident for both the White and Black populations in the late 1980s and increased thereafter; for body mass index, the shift to high rates of change started in both groups in the late 1990s, especially in the middle income quintiles. Our results support use of the haldane as a supplemental metric to place changes in population health and health inequities in a larger biological and historical context.

Quantification of high-specificity cyclic diguanylate signaling

Cyclic di-GMP (c-di-GMP) is a second messenger molecule that regulates the transition between sessile and motile lifestyles in bacteria. Bacteria often encode multiple diguanylate cyclase (DGC) and phosphodiesterase (PDE) enzymes that produce and degrade c-di-GMP, respectively. Because of multiple inputs into the c-di-GMP-signaling network, it is unclear whether this system functions via high or low specificity. High-specificity signaling is characterized by individual DGCs or PDEs that are specifically associated with downstream c-di-GMP-mediated responses. In contrast, low-specificity signaling is characterized by DGCs or PDEs that modulate a general signal pool, which, in turn, controls a global c-di-GMP-mediated response. To determine whether c-di-GMP functions via high or low specificity in Vibrio cholerae, we correlated the in vivo c-di-GMP concentration generated by seven DGCs, each expressed at eight different levels, to the c-di-GMP-mediated induction of biofilm formation and transcription. There was no correlation between total intracellular c-di-GMP levels and biofilm formation or gene expression when considering all states. However, individual DGCs showed a significant correlation between c-di-GMP production and c-di-GMP-mediated responses. Moreover, the rate of phenotypic change versus c-di-GMP concentration was significantly different between DGCs, suggesting that bacteria can optimize phenotypic output to c-di-GMP levels via expression or activation of specific DGCs. Our results conclusively demonstrate that c-di-GMP does not function via a simple, low-specificity signaling pathway in V. cholerae.

Testing convergent and parallel adaptations in talpids humeral mechanical performance by means of geometric morphometrics and finite element analysis

The shape and mechanical performance in Talpidae humeri were studied by means of Geometric Morphometrics and Finite Element Analysis, including both extinct and extant taxa. The aim of this study was to test whether the ability to dig, quantified by humerus mechanical performance, was characterized by convergent or parallel adaptations in different clades of complex tunnel digger within Talpidae, that is, Talpinae+Condylura (monophyletic) and some complex tunnel diggers not belonging to this clade. Our results suggest that the pattern underlying Talpidae humerus evolution is evolutionary parallelism. However, this insight changed to true convergence when we tested an alternative phylogeny based on molecular data, with Condylura moved to a more basal phylogenetic position. Shape and performance analyses, as well as specific comparative methods, provided strong evidence that the ability to dig complex tunnels reached a functional optimum in distantly related taxa. This was also confirmed by the lower phenotypic variance in complex tunnel digger taxa, compared to non-complex tunnel diggers. Evolutionary rates of phenotypic change showed a smooth deceleration in correspondence with the most recent common ancestor of the Talpinae+Condylura clade.

Cultivation as slow evolutionary entanglement: comparative data on rate and sequence of domestication

Recent studies have suggested that domestication was a slower evolutionary process than was previously thought. We address this issue by quantifying rates of phenotypic change in crops undergoing domestication, including five crops from the Near East (Triticum monococcum, T. dicoccum, Hordeum vulgare, Pisum sativum, Lens culinaris) and six crops from other regions (Oryza sativa, Pennisetum glaucum, Vigna radiata, Cucumis melo, Helianthus annus, Iva annua). We calculate rates using the metrics of darwin units and haldane units, which have been used in evolutionary biology, and apply this to data on non-shattering cereal spikelets and seed size. Rates are calculated by considering data over a 4,000-year period from archaeological sites in the region of origin, although we discuss the likelihood that a shorter period of domestication (1,000–2,000) years may be more appropriate for some crops, such as pulses. We report broadly comparable rates of change across all the crops and traits considered, and find that these are close to the averages and median values reported in various evolutionary biological studies. Nevertheless, there is still variation in rates between domesticates, such as melon seeds increasing at twice the rate of cereals, and between traits, such as non-shattering evolving faster than grain size. Such comparisons underline the utility of a quantitative approach to domestication rates, and the need to develop larger datasets for comparisons between crops and across regions.

What Invasive Species Reveal about the Rate and Form of Contemporary Phenotypic Change in Nature

Biological invasions are opportunities to gain insight into fundamental evolutionary questions, because reproductive isolation and sudden alterations in selection pressures are likely to lead to rapid evolutionary change. Here I investigate the role played by invasive species in revealing the rate and form of contemporary phenotypic change in wild populations by expanding a database of more than 5,500 rates of phenotypic change from 90 species of plants and animals. Invasive species are frequently used as model organisms and thus contribute disproportionately to available rates of phenotypic change. However, the preponderance of these rates is the consequence of extensive study in a small number of species. I found mixed evidence to support the hypothesis that phenotypic change is associated with time depending on the metric of choice (i.e., darwins or haldanes). Insights from both invasive and native species provide evidence for abrupt phenotypic change and suggest that the environment plays a potentially important role in driving trait change in wild populations, although the environmental influence on the observed trajectories remains unclear. Thus, future work should continue to seek an understanding of the mechanistic underpinnings--both genetic and environmental--of how phenotypic variation allows populations to adapt to rapidly changing global environments.

Life history change in commercially exploited fish stocks: an analysis of trends across studies.

Age and size at maturation have declined dramatically in many commercial fish stocks over the past few decades – changes that have been widely attributed to fishing pressure. We performed an analysis of such trends across multiple studies, to test for the consistency of life history changes under fishing, and for their association with the intensity of exploitation (fishing mortality rate). We analyzed 143 time series from 37 commercial fish stocks, the majority of which originated from the North Atlantic. Rates of phenotypic change were calculated for two traditional maturation indices (length and age at 50% maturity), as well as for probabilistic maturation reaction norms (PMRNs). We found that all three indices declined in heavily exploited populations, and at a rate that was strongly correlated with the intensity of fishing (for length at 50% maturity and PMRNs). These results support previous assertions that fishing pressure is playing a major role in the life history changes observed in commercial fish stocks. Rates of change were as strong for PMRNs as for age and size at 50% maturity, which is consistent with the hypothesis that fishing-induced phenotypic changes can sometimes have a genetic basis.

Does harvest select for maladaptation in an increasingly variable world?

For several plant and animal species, Darimont et al. (1) present compelling evidence that rates of phenotypic change driven by human harvest far outpace those driven by other selective forces. From a life-history perspective, commercial and trophy harvesting also resulted in smaller size/earlier age at first reproduction, smaller adult body size (sometimes associated with shorter lifespan), and increased reproductive investment. Selection for these traits can mold life histories with faster reproductive tempos that, not surprisingly, can increase maximum yield (in numbers of individuals) under the assumption of a constant environment. In a world in which climatic conditions are predicted to become increasingly variable (2), however, commercial and trophy harvesting practices may be culling the very traits that would be most adaptive in the future.

Changes in selection and evolutionary responses in migratory brown trout following the construction of a fish ladder.

Brown trout (Salmo trutta) are extensively harvested and its habitat highly influenced by human encroachments. Using a 40-year time series of mark–recapture data we estimate vital rates for a piscivorous trout population. This population spawns upstream of a waterfall, which historically acted as a migration barrier for smaller trout. In 1966, the waterfall was dammed and a fish ladder constructed. All fish ascending the fish ladder were individually tagged and measured for a variety of traits. The fish ladder overall favoured access to upstream spawning areas for middle-sized trout, resulting in stabilizing selection acting on size at spawning. Over time, natural and fishing mortality have varied, with fishing mortality generally decreasing and natural mortality increasing. The average and, particularly, variance in size-at-first-spawning, and growth rates during the first years of lake residence have all decreased over the 1966–2003 period. These changes are all consistent with a shift from directional to stabilizing selection on age and size at spawning. Estimated rates of phenotypic change are relatively high, in particular for size at first spawning, adding further support for the growing notion that human interference may lead to rapid life-history trait evolution.

Human influences on rates of phenotypic change in wild animal populations

Human activities can expose populations to dramatic environmental perturbations, which may then precipitate adaptive phenotypic change. We ask whether or not phenotypic changes associated with human-disturbed (anthropogenic) contexts are greater than those associated with more 'natural' contexts. Our meta-analysis is based on more than 3000 rates of phenotypic change in 68 'systems', each representing a given species in a particular geographical area. We find that rates of phenotypic change are greater in anthropogenic contexts than in natural contexts. This difference may be influenced by phenotypic plasticity - because it was evident for studies of wild-caught individuals (which integrate both genetic and plastic effects) but not for common-garden or quantitative genetic studies (which minimize plastic effects). We also find that phenotypic changes in response to disturbance can be remarkably abrupt, perhaps again because of plasticity. In short, humans are an important agent driving phenotypic change in contemporary populations. Although these changes sometimes have a genetic basis, our analyses suggest a particularly important contribution from phenotypic plasticity.

NEUTRAL THEORY, PHYLOGENIES, AND THE RELATIONSHIP BETWEEN PHENOTYPIC CHANGE AND EVOLUTIONARY RATES

The neutral theory of molecular evolution predicts that rates of phenotypic change are largely independent from genotypic change. A recent study by Bromham et al. (2002) confirmed this expectation, finding no evidence for correlated phenotypic and molecular evolutionary rates in animals. We reevaluate this hypothesis, sampling at different taxonomic levels in plants and animals, using Bayesian inference to reconstruct phylogenetic trees and estimate rates of molecular evolution. We use independent contrasts in branch lengths to maximize the information extracted from each of the trees and nodal posterior probabilities to assess the influence of phylogenetic error. Our results indicate that in vascular plants between 2% and 11% of the variation in phenotypic rates of change can be explained by the rate of genotypic change. These results may be explained by the idea that processes that affect general evolutionary rates, such as body size, may also be expected to influence rates of morphological change.

Mutation rates: estimating phase variation rates when fitness differences are present and their impact on population structure.

Phase variation is a mechanism of ON-OFF switching that is widely utilized by bacterial pathogens. There is currently no standardization to how the rate of phase variation is determined experimentally, and traditional methods of mutation rate estimation may not be appropriate to this process. Here, the history of mutation rate estimation is reviewed, describing the existing methods available. A new mathematical model that can be applied to this problem is also presented. This model specifically includes the confounding factors of back-mutation and the influence of fitness differences between the alternate phenotypes. These are central features of phase variation but are rarely addressed, with the result that some previously estimated phase variation rates may have been significantly overestimated. It is shown that, conversely, the model can also be used to investigate fitness differences if mutation rates are approximately known. In addition, stochastic simulations of the model are used to explore the impact of 'jackpot cultures' on the mutation rate estimation. Using the model, the impact of realistic rates and selection on population structure is investigated. In the absence of fitness differences it is predicted that there will be phenotypic stability over many generations. The rate of phenotypic change within a population is likely, therefore, to be principally determined by selection. A greater insight into the population dynamics of mutation rate processes can be gained if populations are monitored over successive time points.

Simulation of responses of community structure to species interactions driven by phenotypic change

We developed a community model which considers the effect of phenotype on species interaction in order to elucidate general relationships between phenotype, species interactions and community structure. The model consists of community matrices with density-dependent species interactions and a limit on the total population of each species. A general natural pattern forms the basis of the model: organisms which are most similar compete, those which are less similar may enter into a predator-prey relationship, and those which are most different may be mutualistic. In this model, contrary to some previously published studies, increasing the number of species increased stability of community matrices. The rate of change in phenotype was varied to assess the response of community characteristics. At the highest rate of random phenotypic change there were the most species; the minimum number of species was found at intermediate rates of change. The models were run in the absence of predation, competition, or mutualism. The absence of mutualism led to more extinction. The absence of competition caused communities to quickly reach a population ceiling. Results suggest that it is extremely important to understand the relative occurrence of mutualism and competition in natural communities. Furthermore, the rate of phenotypic change could be an important but subtle determinant of community structure.

Rate of evolution slowed by a dormant propagule pool

Theoretical models of plant seed banks and common sense suggest that stores of dormant propagules must slow down the rate of genetic change1,2 because they sequester a substantial fraction of the gene pool from the influence of microevolutionary processes in each generation. The magnitude of the effect must represent a balance between the extent of selection and the fraction of the dormant pool that returns to the active population in each generation (and the other microevolutionary processes of migration, drift and mutation). For most populations, in which to observe the action of selection is difficult in itself, detecting the added influence of a dormant propagule pool will be more difficult still. Here we report the effect of hatching of diapausing eggs from lake sediments on the rate of phenotypic change in two populations of the freshwater copepod, Diaptomus sanguineus. When the input of new eggs to the sediments was eliminated by a brief but intense two-year appearance of predators, the role of dormant stages in slowing evolution was clearly seen.