Exploring possible human influences on the evolution of Darwin's finches

Humans are an increasingly common influence on the evolution of natural populations. Potential arenas of influence include altered evolutionary trajectories within populations and modifications of the process of divergence among populations. We consider this second arena in the medium ground finch (Geospiza fortis) on Santa Cruz Island, Galápagos, Ecuador. Our study compared the G. fortis population at a relatively undisturbed site, El Garrapatero, to the population at a severely disturbed site, Academy Bay, which is immediately adjacent to the town of Puerto Ayora. The El Garrapatero population currently shows beak size bimodality that is tied to assortative mating and disruptive selection, whereas the Academy Bay population was historically bimodal but has lost this property in conjunction with a dramatic increase in local human population density. We here evaluate potential ecological-adaptive drivers of the differences in modality by quantifying relationships between morphology (beak and head dimensions), functional performance (bite force), and environmental characteristics (diet). Our main finding is that associations among these variables are generally weaker at Academy Bay than at El Garrapatero, possibly because novel foods are used at the former site irrespective of individual morphology and performance. These results are consistent with the hypothesis that the rugged adaptive landscapes promoting and maintaining diversification in nature can be smoothed by human activities, thus hindering ongoing adaptive radiation.     

Disruptive selection in a bimodal population of Darwin's finches

A key part of the ecological theory of adaptive radiation is disruptive selection during periods of sympatry. Some insight into this process might be gained by studying populations that are bimodal for dual-context traits, i.e. those showing adaptive divergence and also contributing to reproductive isolation. A population meeting these criteria is the medium ground finch (Geospiza fortis) of El Garrapatero, Santa Cruz Island, Galápagos. We examined patterns of selection in this population by relating individual beak sizes to interannual recaptures during a prolonged drought. Supporting the theory, disruptive selection was strong between the two beak size modes. We also found some evidence of selection against individuals with the largest and smallest beak sizes, perhaps owing to competition with other species or to gaps in the underlying resource distribution. Selection may thus simultaneously maintain the current bimodality while also constraining further divergence. Spatial and temporal variation in G. fortis bimodality suggests a dynamic tug of war among factors such as selection and assortative mating, which may alternatively promote or constrain divergence during adaptive radiation.     

Acoustic discrimination of sympatric morphs in Darwin's finches: a behavioural mechanism for assortative mating?

Populations with multiple morphological or behavioural types provide unique opportunities for studying the causes and consequences of evolutionary diversification. A population of the medium ground finch (Geospiza fortis) at El Garrapatero on Santa Cruz Island, Galápagos, features two beak size morphs. These morphs produce acoustically distinctive songs, are subject to disruptive selection and mate assortatively by morph. The main goal of the present study was to assess whether finches from this population are able to use song as a cue for morph discrimination. A secondary goal of this study was to evaluate whether birds from this population discriminate songs of their own locality versus another St Cruz locality, Borrero Bay, approximately 24 km to the NW. I presented territorial males with playback of songs of their own morph, of the other morph, and of males from Borrero Bay. Males responded more strongly to same-morph than to other-morph playbacks, showing significantly shorter latencies to flight, higher flight rates and closer approaches to the playback speaker. By contrast, I found only minor effects of locality on responsiveness. Evidence for morph discrimination via acoustic cues supports the hypothesis that song can serve as a behavioural mechanism for assortative mating and sympatric evolutionary divergence.     

A geometric morphometric appraisal of beak shape in Darwin's finches

Beak size and shape in Darwin's finches have traditionally been quantified using a few univariate measurements (length, depth, width). Here we show the improved inferential resolution of geometric morphometric methods, as applied to three hierarchical levels: (i) among seven species on Santa Cruz Island, (ii) among different sites on Santa Cruz for a single species (Geospiza fortis), and (iii) between large and small beak size morphs of G. fortis at one site (El Garrapatero). Our results support previous studies in finding an axis of shape variation (long/shallow/pointy vs. short/deep/blunt) that separates many of the species. We also detect additional differences among species in the relative sizes and positions of the upper and lower mandibles and in curvature of the mandibles. Small-scale, but potentially relevant, shape variation was also detected among G. fortis from different sites and between sympatric beak size morphs. These results suggest that adaptation to different resources might contribute to diversification on a single island.     

Population Size Affects Adaptation in Complex Ways: Simulations on Empirical Adaptive Landscapes

Do large populations always outcompete smaller ones? Does increasing the mutation rate have a similar effect to increasing the population size, with respect to the adaptation of a population? How important are substitutions in determining the adaptation rate? In this study, we ask how population size and mutation rate interact to affect adaptation on empirical adaptive landscapes. Using such landscapes, we do not need to make many ad hoc assumption about landscape topography, such as about epistatic interactions among mutations or about the distribution of fitness effects. Moreover, we have a better understanding of all the mutations that occur in a population and their effects on the average fitness of the population than we can know in experimental studies. Our results show that the evolutionary dynamics of a population cannot be fully explained by the population mutation rate \(N\mu\); even at constant \(N\mu\), there can be dramatic differences in the adaptation of populations of different sizes. Moreover, the substitution rate of mutations is not always equivalent to the adaptation rate, because we observed populations adapting to high adaptive peaks without fixing any mutations. Finally, in contrast to some theoretical predictions, even on the most rugged landscapes we study, small population size is never an advantage over larger population size. These result show that complex interactions among multiple factors can affect the evolutionary dynamics of populations, and simple models should be taken with caution.     

Density dependence, lifespan and the evolutionary dynamics of longevity

Longevity is a life-history trait that is shaped by natural selection. Evolution will shape mortality trajectories and lifespans, but until now the evolutionary analysis of longevity is based principally on a density-independent (Euler-Lotka) framework. The effects of density dependence on the evolution of lifespan and mortality remain largely unexplored. We investigate the influence of different population demographies on the evolution of longevity, and show how these can be linked to adaptive radiations. We present a range of models to explore the intraspecific and interspecific density effects on longevity and, consequently, diversification. We show how the magnitude, type, and timing of mutation can also affect fitness, invasion and diversification. We argue that fitness of alternative strategies under a range of different demographic structures leads to flat, as opposed to rugged, landscapes and that these flat fitness surfaces are important in the evolution of lifespan and senescence.     

Evolutionary advantage of small populations on complex fitness landscapes

Recent experimental and theoretical studies have shown that small asexual populations evolving on complex fitness landscapes may achieve a higher fitness than large ones due to the increased heterogeneity of adaptive trajectories. Here, we introduce a class of haploid three-locus fitness landscapes that allow the investigation of this scenario in a precise and quantitative way. Our main result derived analytically shows how the probability of choosing the path of the largest initial fitness increase grows with the population size. This makes large populations more likely to get trapped at local fitness peaks and implies an advantage of small populations at intermediate time scales. The range of population sizes where this effect is operative coincides with the onset of clonal interference. Additional studies using ensembles of random fitness landscapes show that the results achieved for a particular choice of three-locus landscape parameters are robust and also persist as the number of loci increases. Our study indicates that an advantage for small populations is likely whenever the fitness landscape contains local maxima. The advantage appears at intermediate time scales, which are long enough for trapping at local fitness maxima to have occurred but too short for peak escape by the creation of multiple mutants.     

Evolution in heterogeneous environments: Effects of migration on habitat specialization

Summary Richard Levins introduced fitness sets as a tool for investigating evolution within heterogeneous environments. Evolutionary game theory permits a synthesis and generalization of this approach by considering the evolutionary response of organisms to any scale of habitat heterogeneity. As scales of heterogeneity increase from fine to coarse, the evolutionary stable strategy (ESS) switches from a single generalist species to several species that become increasingly specialized on distinct habitats. Depending upon the organisms' ecology, the switch from one to two species may occur at high migration rates (relatively fine-grained environment), or may only occur at very low migration rates (coarse-grained environment). At the ESS, the evolutionary context of a species is the entire landscape, while its ecological context may be a single habitat.Evolution towards the ESS can be represented with adaptive landscapes. In the absence of frequency-dependence, shifting from a single strategy ESS to a two strategy ESS poses the problem of evolving across valleys in the adaptive surface to occupy new peaks (hence, Sewell Wright's shifting balance theory). Frequency-dependent processes facilitate evolution across valleys. If a system with a two strategy ESS is constrained to possess a single strategy, the population may actually evolve a strategy that minimizes fitness. Because the population now rests at the bottom of a valley, evolution by natural selection can drive populations to occupy both peaks.     

Performance in three shell functions predicts the phenotypic distribution of hard‐shelled turtles

Adaptive landscapes have served as fruitful guides to evolutionary research for nearly a century. Current methods guided by landscape frameworks mostly utilize evolutionary modeling (e.g., fitting data to Ornstein–Uhlenbeck models) to make inferences about adaptive peaks. Recent alternative methods utilize known relationships between phenotypes and functional performance to derive information about adaptive landscapes; this information can then help explain the distribution of species in phenotypic space and help infer the relative importance of various functions for guiding diversification. Here, data on performance for three turtle shell functions–strength, hydrodynamic efficiency, and self‐righting ability–are used to develop a set of predicted performance optima in shell shape space. The distribution of performance optima shows significant similarity to the distribution of existing turtle species and helps explain the absence of shells in otherwise anomalously empty regions of morphospace. The method outperforms a modeling‐based approach in inferring the location of reasonable adaptive peaks and in explaining the shape of the phenotypic distributions of turtle shells. Performance surface‐based methods allow researchers to more directly connect functional performance with macroevolutionary diversification, and to explain the distribution of species (including presences and absences) across phenotypic space.     

The Effect of Bacterial Recombination on Adaptation on Fitness Landscapes with Limited Peak Accessibility

There is ample empirical evidence revealing that fitness landscapes are often complex: the fitness effect of a newly arisen mutation can depend strongly on the allelic state at other loci. However, little is known about the effects of recombination on adaptation on such fitness landscapes. Here, we investigate how recombination influences the rate of adaptation on a special type of complex fitness landscapes. On these landscapes, the mutational trajectories from the least to the most fit genotype are interrupted by genotypes with low relative fitness. We study the dynamics of adapting populations on landscapes with different compositions and numbers of low fitness genotypes, with and without recombination. Our results of the deterministic model (assuming an infinite population size) show that recombination generally decelerates adaptation on these landscapes. However, in finite populations, this deceleration is outweighed by the accelerating Fisher-Muller effect under certain conditions. We conclude that recombination has complex effects on adaptation that are highly dependent on the particular fitness landscape, population size and recombination rate.     

Character displacement as the "best of a bad situation": fitness trade-offs resulting from selection to minimize resource and mate competition

Abstract Character displacement has long been considered a major cause of adaptive diversification. When species compete for resources or mates, character displacement minimizes competition by promoting divergence in phenotypes associated with resource use (ecological character displacement) or mate attraction (reproductive character displacement). In this study, we investigated whether character displacement can also have pleiotropic effects that lead to fitness trade-offs between the benefits of avoiding competition and costs accrued in other fitness components. We show that both reproductive and ecological character displacement have caused spadefoot toads to evolve smaller body size in the presence of a heterospecific competitor. Although this shift in size likely arose as a by-product of character displacement acting to promote divergence between species in mating behavior and larval development, it concomitantly reduces offspring survival, female fecundity, and sexual selection on males. Thus, character displacement may represent the "best of a bad situation" in that it lessens competition, but at a cost. Individuals in sympatry with the displaced phenotype will have higher fitness than those without the displaced trait because they experience reduced competition, but they may have reduced fitness relative to individuals in allopatry. Such a fitness trade-off can limit the conditions under which character displacement evolves and may even increase the risk of "Darwinian extinction" in sympatric populations. Consequently, character displacement may not always promote diversification in the manner that is often expected.     

Genome structure and the benefit of sex

We examine the behavior of sexual and asexual populations in modular multipeaked fitness landscapes and show that sexuals can systematically reach different, higher fitness adaptive peaks than asexuals. Whereas asexuals must move against selection to escape local optima, sexuals reach higher fitness peaks reliably because they create specific genetic variants that "skip over" fitness valleys, moving from peak to peak in the fitness landscape. This occurs because recombination can supply combinations of mutations in functional composites or "modules," that may include individually deleterious mutations. Thus when a beneficial module is substituted for another less-fit module by sexual recombination it provides a genetic variant that would require either several specific simultaneous mutations in an asexual population or a sequence of individual mutations some of which would be selected against. This effect requires modular genomes, such that subsets of strongly epistatic mutations are tightly physically linked. We argue that such a structure is provided simply by virtue of the fact that genomes contain many genes each containing many strongly epistatic nucleotides. We briefly discuss the connections with "building blocks" in the evolutionary computation literature. We conclude that there are conditions in which sexuals can systematically evolve high-fitness genotypes that are essentially unevolvable for asexuals.     

The rank ordering of genotypic fitness values predicts genetic constraint on natural selection on landscapes lacking sign epistasis

Sewall Wright's genotypic fitness landscape makes explicit one mechanism by which epistasis for fitness can constrain evolution by natural selection. Wright distinguished between landscapes possessing multiple fitness peaks and those with only a single peak and emphasized that the former class imposes substantially greater constraint on natural selection. Here I present novel formalism that more finely partitions the universe of possible fitness landscapes on the basis of the rank ordering of their genotypic fitness values. In this report I focus on fitness landscapes lacking sign epistasis (i.e., landscapes that lack mutations the sign of whose fitness effect varies epistatically), which constitute a subset of Wright's single peaked landscapes. More than one fitness rank ordering lacking sign epistasis exists for L > 2 (where L is the number of interacting loci), and I find that a highly statistically significant effect exists between landscape membership in fitness rank-ordering partition and two different proxies for genetic constraint, even within this subset of landscapes. This statistical association is robust to population size, permitting general inferences about some of the characteristics of fitness rank orderings responsible for genetic constraint on natural selection.     

Complex life cycles drive community assembly through immigration and adaptive diversification

Most animals undergo ontogenetic niche shifts during their life. Yet, standard ecological theory builds on models that ignore this complexity. Here, we study how complex life cycles, where juvenile and adult individuals each feed on different sets of resources, affect community richness. Two different modes of community assembly are considered: gradual adaptive evolution and immigration of new species with randomly selected phenotypes. We find that under gradual evolution complex life cycles can lead to both higher and lower species richness when compared to a model of species with simple life cycles that lack an ontogenetic niche shift. Thus, complex life cycles do not per se increase the scope for gradual adaptive diversification. However, complex life cycles can lead to significantly higher species richness when communities are assembled trough immigration, as immigrants can occupy isolated peaks of the dynamic fitness landscape that are not accessible via gradual evolution.     

A population genetics model for multiple quantitative traits exhibiting pleiotropy and epistasis

We study a population genetics model of an organism with a genome of L(tot)loci that determine the values of T quantitative traits. Each trait is controlled by a subset of L loci assigned randomly from the genome. There is an optimum value for each trait, and stabilizing selection acts on the phenotype as a whole to maintain actual trait values close to their optima. The model contains pleiotropic effects (loci can affect more than one trait) and epistasis in fitness. We use adaptive walk simulations to find high-fitness genotypes and to study the way these genotypes are distributed in sequence space. We then simulate the evolution of haploid and diploid populations on these fitness landscapes and show that the genotypes of populations are able to drift through sequence space despite stabilizing selection on the phenotype. We study the way the rate of drift and the extent of the accessible region of sequence space is affected by mutation rate, selection strength, population size, recombination rate, and the parameters L and T that control the landscape shape. There are three regimes of the model. If LTL(tot), there are many small peaks that can be spread over a wide region of sequence space. Compensatory neutral mutations are important in the population dynamics in this case.     

Environmental change exposes beneficial epistatic interactions in a catalytic RNA

Natural selection drives populations of individuals towards local peaks in a fitness landscape. These peaks are created by the interactions between individual mutations. Fitness landscapes may change as an environment changes. In a previous contribution, we discovered a variant of the Azoarcus group I ribozyme that represents a local peak in the RNA fitness landscape. The genotype at this peak is distinguished from the wild-type by four point mutations. We here report ribozyme fitness data derived from constructing all possible combinations of these point mutations. We find that these mutations interact epistatically. Importantly, we show that these epistatic interactions change qualitatively in the three different environments that we studied. We find examples where the relative fitness of a ribozyme can change from neutral or negative in one environment, to positive in another. We also show that the fitness effect of a specific GC-AU base pair switch is dependent on both the environment and the genetic context. Moreover, the mutations that we study improve activity at the cost of decreased structural stability. Environmental change is ubiquitous in nature. Our results suggest that such change can facilitate adaptive evolution by exposing new peaks of a fitness landscape. They highlight a prominent role for genotype-environment interactions in doing so.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.     

Biogeography of species richness gradients: linking adaptive traits,demography and diversification

Here we review how adaptive traits contribute to the emergence and maintenance of species richness gradients through their influence on demographic and diversification processes. We start by reviewing how demographic dynamics change along species richness gradients. Empirical studies show that geographical clines in population parameters and measures of demographic variability are frequent along latitudinal and altitudinal gradients. Demographic variability often increases at the extremes of regional species richness gradients and contributes to shape these gradients. Available studies suggest that adaptive traits significantly influence demographic dynamics, and set the limits of species distributions. Traits related to thermal tolerance, resource use, phenology and dispersal seem to play a significant role. For many traits affecting demography and/or diversification processes, complex mechanistic approaches linking genotype, phenotype and fitness are becoming progressively available. In several taxa, species can be distributed along adaptive trait continuums, i.e. a main axis accounting for the bulk of inter‐specific variation in some correlated adaptive traits. It is shown that adaptive trait continuums can provide useful mechanistic frameworks to explain demographic dynamics and diversification in species richness gradients. Finally, we review the existence of sequences of adaptive traits in phylogenies, the interactions of adaptive traits and community context, the clinal variation of traits across geographical gradients, and the role of adaptive traits in determining the history of dispersal and diversification of clades. Overall, we show that the study of demographic and evolutionary mechanisms that shape species richness gradients clearly requires the explicit consideration of adaptive traits. To conclude, future research lines and trends in the field are briefly outlined.     

Variation in behavioral traits of two frugivorous mammals may lead to differential responses to human disturbance

Human activities can lead to a shift in wildlife species’ spatial distribution. Understanding the specific effects of human activities on ranging behavior can improve conservation management of wildlife populations in human‐dominated landscapes. This study evaluated the effects of forest use by humans on the spatial distribution of mammal species with different behavioral adaptations, using sympatric western lowland gorilla and central chimpanzee as focal species. We collected data on great ape nest locations, ecological and physical variables (habitat distribution, permanent rivers, and topographic data), and anthropogenic variables (distance to trails, villages, and a permanent research site). Here, we show that anthropogenic variables are important predictors of the distribution of wild animals. In the resource model, the distribution of gorilla nests was predicted by nesting habitat distribution, while chimpanzee nests were predicted first by elevation followed by nesting habitat distribution. In the anthropogenic model, the major predictors of gorilla nesting changed to human features, while the major predictors of chimpanzee nesting remained elevation and the availability of their preferred nesting habitats. Animal behavioral traits (body size, terrestrial/arboreal, level of specialization/generalization, and competitive inferiority/superiority) may influence the response of mammals to human activities. Our results suggest that chimpanzees may survive in human‐encroached areas whenever the availability of their nesting habitat and preferred fruits can support their population, while a certain level of human activities may threaten gorillas. Consequently, the survival of gorillas in human‐dominated landscapes is more at risk than that of chimpanzees. Replicating our research in other sites should permit a systematic evaluation of the influence of human activity on the distribution of mammal populations. As wild animals are increasingly exposed to human disturbance, understanding the resulting consequences of shifting species distributions due to human disturbance on animal population abundance and their long‐term survival will be of growing conservation importance.     

FOUNDER EFFECTS AND PEAK SHIFTS WITHOUT GENETIC DRIFT: ADAPTIVE PEAK SHIFTS OCCUR EASILY WHEN ENVIRONMENTS FLUCTUATE SLIGHTLY

Two similar evolutionary theories, the shifting balance theory and founder-flush models, invoke random genetic drift to allow evolution on complex adaptive landscapes. These models, in their usual incarnations, deal with fitness as a static entity, and the probability of transition from one form to another is predicted to be quite small by analysis of these models. Fitness itself can change, however, and the amount of change in the parameters of the fitness functions required to allow deterministic evolution to new adaptive peaks is very small. The probability of environmental changes sufficient to allow substantial morphological evolution or reproductive isolation is large relative to the probability that similar changes could occur by processes requiring genetic drift, even with very small population sizes. The rapid evolution or speciation following a population founding event is more closely linked with environmental changes than genetic drift.