Multiple Adaptive Peaks Research Articles

Morphological variation associated with trophic niche expansion within a lake population of a benthic fish

Ecological theory suggests that generalist species should have traits with multiple adaptive peaks. Consequently, in heterogeneous environments such adaptive landscapes may lead to phenotypic divergence that becomes fixed in populations via reproductive isolation, thus driving speciation. However, contrary to this expectation, the process of ecological diversification in wild populations is not always associated with obvious trait divergence and reproductive isolation due to some ecological and geographic constrains. To examine the ecological conditions that promote (or inhibit) divergence is quite important to improve our understanding of the underlying mechanisms. Here we examine how the patterns of trait variation (divergence/non-divergence) are determined in relation to ecological niche expansion and gene flow using a benthic fish, Pseudogobio esocinus, in the Lake Biwa system, Japan. The fish exhibited various patterns of morphological variation in mouth parts among populations. Lake fish tended to have a smaller mouth compared with river fish and also showed remarkable individual variations within some local samples. Lake fish utilized chironomid larvae as the primary prey, as in riverine fish. But, fish with smaller and narrower mouths utilized significantly higher proportions of amphipods (a novel prey unique to the lake) as their secondary prey. Microsatellite analysis detected no genetic structuring in the Lake Biwa catchment, suggesting no reproductive separation among eco-morphologically divergent individuals. Our results exemplify population niche expansion associated with continuous eco-morphological variation without divergence, and provide insights into the role of non-discrete diversification for thriving in heterogeneous environments.

Convergent Evolution of Claw Shape in a Transcontinental Lizard Radiation.

Species occupying similar selective environments often share similar phenotypes as the result of natural selection. Recent discoveries, however, have led to the understanding that phenotypes may also converge for other reasons than recurring selection. We argue that the vertebrate claw system constitutes a promising but understudied model system for testing the adaptive nature of phenotypic, functional, and genetic convergence. In this study, we combine basic morphometrics and advanced techniques in form analysis to examine claw shape divergence in a transcontinental lizard radiation (Lacertidae). We find substantial interspecific variation in claw morphology and phylogenetic comparative statistics reveal a strong correlation with structural habitat use: ground-dwelling species living in open areas are equipped with long, thick, weakly curved, slender-bodied claws, whereas climbing species carry high, short, strongly curved, full-bodied claws. Species occupying densely vegetated habitats tend to carry intermediately shaped claws. Evolutionary models suggest that claw shape evolves toward multiple adaptive peaks, with structural habitat use pulling species toward a specific selective optimum. Contrary to findings in several other vertebrate taxa, our analyses indicate that environmental pressures, not phylogenetic relatedness, drive convergent evolution of similarly shaped claws in lacertids. Overall, our study suggests that lacertids independently evolved similarly shaped claws as an adaptation to similar structural environments in order to cope with the specific locomotory challenges posed by the habitat. Future biomechanical studies that link form and function in combination with genomic and development research will prove valuable in better understanding the adaptive significance of claw shape divergence.

Ecological niche and phylogeny explain distribution of seed mass in the central European flora

Seed size is a crucial life‐history trait determining the amount of reserves that are available to establishing seedlings. The most frequently observed patterns in seed size distribution are a higher frequency of large‐seeded species in shaded habitats and a positive correlation of seed size with plant size. We analysed to what extent realised niche dimensions, as expressed by Ellenberg indicator values and plant functional traits such as plant height and life form, explained seed mass variation in the central European flora. By including information on phylogenetic relatedness of the species, not only contemporary ecology but also the evolutionary history of plant species could be taken into account. Seed mass evolution was slow and was best explained by selection‐inertia models with multiple adaptive peaks as a function of either habitat or life form. The highest seed mass optima were observed in the deciduous forest and saltwater and seashore habitats, and in phanerophytes in case of models with optima as a function of life form. The analyses showed that Ellenberg values were more important than habitat and life form in explaining seed mass distribution in the central European flora. The often observed relation between shade and large seeds was also evident in our study, but we found an equally important relation between large seeds and drought and a positive relation between seed mass and salinity. Our results indicate that not only plant size and competition for light but a complex set of factors influence the ecology of seed size, and that a more precise delineation of species’ niches improves the understanding of seed size evolution.

Climatic niche evolution in the Andean genus Menonvillea (Cremolobeae: Brassicaceae)

Fil: Salariato, Diego Leonel. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Instituto de Botanica Darwinion. Academia Nacional de Ciencias Exactas, Fisicas y Naturales. Instituto de Botanica Darwinion; Argentina

Selection towards different adaptive optima drove the early diversification of locomotor phenotypes in the radiation of Neotropical geophagine cichlids

BackgroundSimpson envisaged a conceptual model of adaptive radiation in which lineages diversify into “adaptive zones” within a macroevolutionary adaptive landscape. However, only a handful of studies have empirically investigated this adaptive landscape and its consequences for our interpretation of the underlying mechanisms of phenotypic evolution. In fish radiations the evolution of locomotor phenotypes may represent an important dimension of ecomorphological diversification given the implications of locomotion for feeding and habitat use. Neotropical geophagine cichlids represent a newly identified adaptive radiation and provide a useful system for studying patterns of locomotor diversification and the implications of selective constraints on phenotypic divergence in general.ResultsWe use multivariate ordination, models of phenotypic evolution and posterior predictive approaches to investigate the macroevolutionary adaptive landscape and test for evidence of early divergence of locomotor phenotypes in Geophagini. The evolution of locomotor phenotypes was characterized by selection towards at least two distinct adaptive peaks and the early divergence of modern morphological disparity. One adaptive peak included the benthic and epibenthic invertivores and was characterized by fishes with deep, laterally compressed bodies that optimize precise, slow-swimming manoeuvres. The second adaptive peak resulted from a shift in adaptive optima in the species-rich ram-feeding/rheophilic Crenicichla-Teleocichla clade and was characterized by species with streamlined bodies that optimize fast starts and rapid manoeuvres. Evolutionary models and posterior predictive approaches favoured an early shift to a new adaptive peak over decreasing rates of evolution as the underlying process driving the early divergence of locomotor phenotypes.ConclusionsThe influence of multiple adaptive peaks on the divergence of locomotor phenotypes in Geophagini is compatible with the expectations of an ecologically driven adaptive radiation. This study confirms that the diversification of locomotor phenotypes represents an important dimension of phenotypic evolution in the geophagine adaptive radiation. It also suggests that the commonly observed early burst of phenotypic evolution during adaptive radiations may be better explained by the concentration of shifts to new adaptive peaks deep in the phylogeny rather than overall decreasing rates of evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0348-7) contains supplementary material, which is available to authorized users.

Evolution of Antibiotic Resistance through a Multi-Peaked Adaptive Landscape

Antibiotic resistance is an evolving threat to public health. Understanding the evolution of antibiotic resistance at the genetic level is critical to develop novel strategies to diagnose and treat antibiotic resistant infections. We recently developed an automated microbial selection device, the “morbidostat”, which is used to study the evolution of antibiotic resistance in dynamically sustained drug selection. The morbidostat adjusts drug concentrations to maintain nearly constant inhibition of bacterial growth even as evolving bacterial populations acquire higher resistance. using the morbidostat and next generation sequencing, we identified striking features in the evolution of trimethoprim resistance in five E. coli populations evolving in parallel. We found that resistance was acquired in a stepwise manner, through multiple mutations almost exclusively restricted to the gene encoding trimethoprim's target, dihydrofolate reductase (DHFR). Multiple distinct genotypes produced very similar trimethoprim resistant phenotypes, with each highly evolved strain each containing four mutations from a set of six possibilities, that were acquired in a non-random order. Never were more than four mutations acquired, despite sustained selection for further increases in drug resistance, indicating that these genotypes were local adaptive peaks.In order to understand how the adaptive landscape of drug resistance contained multiple peaks, all combinatorial sets of adaptive mutations in the DHFR gene (96 strains) were constructed and characterized. These measurements showed that resistance evolves through an almost maximally rugged adaptive landscape with direct and indirect trajectories leading to distinct peaks. The ruggedness was not explained by pairwise incompatibilities between mutations, instead indicating ‘high-order' genetic interactions between mutations. These high-order interactions were responsible for the existence of multiple adaptive peaks. One mutation was seen to have the power to control the adaptive landscape: its presence or absence largely defined the ruggedness or smoothness of the adaptive landscape.

Trait evolution in an individual-based model of herbaceous vegetation

Many theoretical studies of evolution are based upon the concepts of the evolutionary stable strategy and optimal life-history solutions. An individual based model of vegetation is used to simulate life-history evolution under two different sets of environmental conditions. At one level the results suggest that optimal life-history solutions do appear to evolve. At the end of the simulations the vegetation that evolved in a fertile and uncut environment was taller, thinner and germinated later than that which developed in a less fertile and cut habitat. However, between simulation variation was observed to be high, particularly for the parameter regulating the timing of reproduction, and it showed no indication of reaching fixation. When this trait was prevented from mutating, the variances of other traits were seen to increase. Although at the population level between simulation variation was high, some traits achieved a degree of stability within simulations, suggesting that multiple adaptive peaks may be being approached. However, there was little evidence of trait fixation occurring within the most abundant ‘genotype’. It is considered that frequency dependent selection/Red Queen dynamics may be acting to prevent the most abundant ‘genotype’ from reaching fixation. It is argued that if such processes prevent optimal genetic solutions from being achieved then the search for evolutionary stable strategies within the evolution of life-histories may be over simplistic.

Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat.

Natural selection tends to promote the divergence of populations living in different environments. Even in identical environments, however, replicate populations may diverge if they find alternative adaptive solutions. We describe the evolution of 18 bacterial populations (Comamonas sp.) founded from a single progenitor genotype and propagated separately for 1000 generations in two distinct environments, one physically unstructured (mass-action liquid) and the other structured (agar surfaces). Phenotypic diversity, as reflected in colony morphology, was greater in the structured habitat than in the unstructured habitat. More importantly, the trajectories for mean fitness, as measured by competition against the common ancestor, were more divergent for populations in the structured habitat than those in the unstructured habitat. Structured environments may accelerate evolutionary diversification by promoting genetic polymorphisms within populations, thereby increasing the complexity of genetic constraints that allow divergence among replicate populations.

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. II. ANALYSIS OF SELECTION AND RANDOM CHANGE IN FOSSIL SPECIES USING RECONSTRUCTED GENETIC PARAMETERS.

The roles of natural selection and random genetic change in the punctuated phenotypic evolution of eight Miocene-Pliocene tropical American species of the cheilostome bryozoan Metrarabdotos are analyzed by quantitative genetic methods. Trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance are similar to those previously obtained for living species of the cheilostome Stylopoma using breeding data. The hypothesis that differences in skeletal morphology between species of Metrarabdotos are entirely due to mutation and genetic drift cannot be rejected for reasonable rates of mutation maintained for periods brief enough to account for the geologically abrupt appearances of these species in the fossil record. Except for one pair of species, separated by the largest morphologic distance, directional selection acting alone would require unrealistically high rates of selective mortality to be maintained for these periods. Thus, directional selection is not strongly implicated in the divergence of Metrarabdotos species. Within species, rates of net phenotypic change are slow enough to require stabilizing selection, but mask large, relatively rapid fluctuations, all of which, however, can be attributed to chance departures from the mean phenotype by mutation and genetic drift, rather than to tracking environmental fluctuation by directional selection. The results are consistent with genetic models involving shifts between multiple adaptive peaks on which phenotypes remain more or less static through long-term stabilizing selection. Regardless of the degree to which directional selection may be involved in peak shifts, phenotypic differentiation is thus related to processes different than the pervasive stabilizing selection acting within species.

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. I. RATE TESTS FOR RANDOM CHANGE VERSUS SELECTION IN DIFFERENTIATION OF LIVING SPECIES.

The possible roles of random genetic change and natural selection in bryozoan speciation were analyzed using quantitative genetic methods on breeding data for traits of skeletal morphology in two closely related species of the cheilostome Stylopoma. The hypothesis that morphologic differences between the species are caused entirely by mutation and genetic drift could not be rejected for reasonable rates of mutation maintained for as few as 103 to 104 generations. Divergence times this short or shorter are consistent with the abrupt appearances of many invertebrate species in the fossil record, commonly followed by millions of years of morphologic stasis. To produce these differences over 103 generations or fewer, directional selection acting alone would require unrealistically high levels of minimum selective mortality throughout divergence. Thus, selection is unnecessary to explain the divergence of these species, except as a means of accelerating the effects of random genetic change on shorter time scales (directional selection), or decelerating them over longer ones (stabilizing selection). These results are consistent with a variety of models of phenotypic evolution involving random shifts between multiple adaptive peaks. Similar results were obtained by substituting trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance in place of the values based on breeding data. Quantitative genetic analysis of speciation in fossil bryozoan lineages is thus justified.

PATTERNS OF SELECTION ON PHYTOPHAGE RESISTANCE IN IPOMOEA PURPUREA.

Adaptive landscapes with multiple peaks have been invoked to explain a variety of evolutionary phenomenona, including the divergence of populations in mean phenotype (Futuyma 1986), the evolution of coadapted gene complexes (Charlesworth and Charlesworth, 1976; Turner 1977) and the rapid spread of favorable gene combinations by group selection and genetic drift (Wright 1932, 1977, 1978). Nevertheless, definitive examples from natural populations of adaptive surfaces with multiple peaks are few (but see Lewontin and White 1960; Smith 1990; Wiggins 1991; Brodie 1992), particularly for suites of quantitative characters (Lande and Arnold 1983). It is thus unclear how commonly natural populations are characterized by multiple adaptive peaks; and hence, in general what the potential is for multiple peaks to influence evolutionary processes in natural populations. Addressing this issue will require estimating the form of the adaptive surfaces of a variety of organisms (Lande and Arnold 1983). In this report we describe the adaptive surface corresponding to a suite of resistance traits in the annual morning glory, Ipomoea purpurea. Several investigators have suggested that the evolution of resistance against particular parasites (pathogens, herbivores) may be influenced by the presence of, and the pattern of selection imposed by, other types of parasites (Janzen 1980; Fox 1981; Simms and Rausher 1987; Gould 1988; Pilson 1992). Because little empirical evidence bearing on this issue exists, however, it is far from clear whether, in general, resistances to different parasites evolve independently in natural populations. The presence of multiple adaptive peaks in the adaptive surface associated with resistance traits could generate nonindependence if different combinations of resistance were associated with different peaks (e.g., one favored combination is resistance to one parasite but susceptibility to another, while another favored combination is the opposite). We examined this possibility for one system by quantifying the adaptive surface for resistance to two parasites in Ipomoea purpurea.

Functional significance of preserved color patterns of mollusks from the Gosport Sand (Eocene) of Alabama

The excellent preservation of the molluscan fauna from the Gosport Sand (Eocene) at Little Stave Creek, Alabama, has made it possible to describe the preserved color patterns of 15 species. In this study the functional significance of these color patterns is tested in the context of the current adaptationist controversy. The pigment of the color pattern is thought to be a result of metabolic waste disposal. Therefore, the presence of the pigment is functional, although the patterns formed by the pigment may or may not have been adaptive. In this investigation the criteria proposed by Seilacher (1972) for testing the functionality of color patterns were applied to the Gosport fauna and the results compared with life mode as interpreted from knowledge of extant relatives and functional morphology. Using Seilacher's criteria of little ontogenetic and intraspecific variability, the color patterns appear to have been functional. However, the functional morphology studies indicate an infaunal life mode which would preclude functional color patterns. Particular color patterns are instead interpreted to be the result of historical factors, such as multiple adaptive peaks or random fixation of alleles, or of architectural constraints including possibly pleiotropy or allometry. The low variability of color patterns, which was noted within species and genera, suggests that color patterns may also serve a useful taxonomic purpose.

Functional significance of preserved color patterns of mollusks from the Gosport Sand (Eocene) of Alabama

The excellent preservation of the molluscan fauna from the Gosport Sand (Eocene) at Little Stave Creek, Alabama, has made it possible to describe the preserved color patterns of 15 species. In this study the functional significance of these color patterns is tested in the context of the current adaptationist controversy. The pigment of the color pattern is thought to be a result of metabolic waste disposal. Therefore, the presence of the pigment is functional, although the patterns formed by the pigment may or may not have been adaptive. In this investigation the criteria proposed by Seilacher (1972) for testing the functionality of color patterns were applied to the Gosport fauna and the results compared with life mode as interpreted from knowledge of extant relatives and functional morphology. Using Seilacher's criteria of little ontogenetic and intraspecific variability, the color patterns appear to have been functional. However, the functional morphology studies indicate an infaunal life mode which would preclude functional color patterns. Particular color patterns are instead interpreted to be the result of historical factors, such as multiple adaptive peaks or random fixation of alleles, or of architectural constraints including possibly pleiotropy or allometry. The low variability of color patterns, which was noted within species and genera, suggests that color patterns may also serve a useful taxonomic purpose.

The dynamics of peak shifts and the pattern of morphological evolution

Recent theoretical results demonstrate that a phenotypic version of Wright's shifting balance theory generates the dynamical pattern of punctuated equilibria. Thus, classical mechanisms of random genetic drift and selection for multiple adaptive peaks produce geologically long periods of relative stasis interrupted occasionally by very brief intervals of rapid change. A simple extension of this theory is made here to encompass developmental constraints between quantitative characters, manifested as phenotypic and genetic correlations between characters. Developmental constraints do not qualitatively alter the dynamical pattern of phenotypic evolution produced by selection and random genetic drift. A quantitative definition of stasis is proposed, based on a common taxonomic practice for recognizing subspecies. From this it is concluded that stasis is not the rule for quantitative measurements of detailed sequences for fossil species throughout most of their existence. Instead, periods of relative stasis are interspersed with gradual fluctuating trends, short intervals of rapid change, and discontinuities of subspecific magnitude.

THE EFFECTS OF INDIVIDUAL VARIATION IN PHYSIOLOGICAL AND MORPHOLOGICAL TRAITS ON THE REPRODUCTIVE CAPACITY OF THE COMMON COCKLEBUR, XANTHIUM STRUMARIUM L.

In studying plant adaptation, physiological ecologists have tended to emphasize the contributions of particular traits to survival under extreme conditions rather than their effects on reproductive success in more moderate environments. We know, for example, a great deal about the physiological and morphological traits that underlie the ability of Atriplex species to grow in arid and saline habitats but virtually nothing about how such traits affect Atriplex reproduction (Osmond et al., 1980). Water use efficiency may critically influence the limits to a plant's survival along an aridity gradient, but within the limits to survival how successfully will individual plants with different water use efficiencies reproduce over their lifetimes? Traits like water use efficiency that draw our attention in studying plant adaptation have arisen at least in part by natural selection acting on these differences in lifetime reproductive success. Within the constraints set by both intrinsic and extrinsic factors (see Gould and Lewontin, 1979), the water use efficiency typical of the individuals reproducing most will predominate in subsequent generations. Therefore to better understand the evolutionary adaptation of plants, we must begin to relate variation in morphological and physiological traits to variation in reproductive success among individual plants growing within their environmental limits. Data on the covariance of vegetative and reproductive traits not only provide some of the clearest evidence for the adaptive significance of traits (CluttonBrock and Harvey, 1979), but can also contribute to the resolution of some current problems in the analysis of evolutionary adaptation. Gould and Lewontin (1979; Lewontin, 1977a, 1977b, 1978) have argued cogently that not all traits are perfectly adapted, and indeed that many may not be adaptations at all. They review evidence that factors like multiple adaptive peaks, founder effects, pleiotropy, linkage disequilibrium, allometric interactions, compensatory allocation of limited resources, and the evolutionary history of an organism can all constrain the attainment of perfect adaptation to an environmental regime. If such constraints have affected the evolution of a particular trait they may be apparent in an analysis of the genotypic and phenotypic variance-covariance matrices among traits that quantitatively characterized an organism (Falconer, 1960; Lande, 1982). These matrices can only be estimated by comparison of natural variation among individuals; once estimated they can be used to predict the direction of microevolution in a particular selection regime (Lande, 1982). Although some would disagree (Stebbins and Ayala, 1981), Gould (1980, 1982) has argued that a new and general theory of evolution is emerging that depends in part on such analyses of the whole organism with its characteristics shaped not only by selection but also by the intrinsic and extrinsic constraints on selection. Mayr (1983) differs with Gould and Lewontin (1979) on a number of points, but he does agree that a renewed emphasis on the whole organism is appropriate. In a similar vein, Harper (1982) has argued that the study of evolutionary processes operating on individual plants will most effectively advance our understanding of plant ecology and plant adaptation.

The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme.

An adaptationist programme has dominated evolutionary thought in England and the United States during the past 40 years. It is based on faith in the power of natural selection as an optimizing agent. It proceeds by breaking an oragnism into unitary 'traits' and proposing an adaptive story for each considered separately. Trade-offs among competing selective demands exert the only brake upon perfection; non-optimality is thereby rendered as a result of adaptation as well. We criticize this approach and attempt to reassert a competing notion (long popular in continental Europe) that organisms must be analysed as integrated wholes, with Baupläne so constrained by phyletic heritage, pathways of development and general architecture that the constraints themselves become more interesting and more important in delimiting pathways of change than the selective force that may mediate change when it occurs. We fault the adaptationist programme for its failure to distinguish current utility from reasons for origin (male tyrannosaurs may have used their diminutive front legs to titillate female partners, but this will not explain why they got so small); for its unwillingness to consider alternatives to adaptive stories; for its reliance upon plausibility alone as a criterion for accepting speculative tales; and for its failure to consider adequately such competing themes as random fixation of alleles, production of non-adaptive structures by developmental correlation with selected features (allometry, pleiotropy, material compensation, mechanically forced correlation), the separability of adaptation and selection, multiple adaptive peaks, and current utility as an epiphenomenon of non-adaptive structures. We support Darwin's own pluralistic approach to identifying the agents of evolutionary change.

GENETIC VARIATION IN AN ASEXUAL SPECIES, THE GARDEN STRAWBERRY

genetic variation, like other attributes, of a population is a product of tem of the organism. WRIGHT (1956) discussed selection in terms of the concept, outlined by him in various earlier papers, of multiple “adaptive peaks” in the potential array of genotypes of a species. In the process he drew a contrast between populations in which reproduction is exclusively biparental and ones in which it is ordinarily asexual but occasionally biparental. He indicates that with biparental reproduction and continuous selection of a constant sort in a relatively stable environment, the expectation in any single panmictic population is a set of coadapted genotypes. These genotypes would all be associated with a single adaptive peak (not necessarily the h’ghest) and coadapted in the sense that new genotypes derived by random intercrossing would have average value about equal to that of the parent genotypes. On the other hand, he pointed out that asexual reproduction allows strong selection among clones (individual genotypes) so that the emphasis is shifted from coadaptation to the excellence (fitness) of the single genotype in its own right. Thus surviving genotypes (clones) are more likely to be associated with different adaptive peaks and to exhibit less coadaptation. The suggested contrast in coadaptation can be illustrated in terms of economic plants. Random intercrossing in an open-pollinated variety of corn yields a new generation about equal in value to the parental generation. However, random crosses among clones of strawberries, potatoes, sugar cane, etc. that have survived as commercial varieties yield progenies of markedly lower value than the parents. The existence of multiple adaptive peaks is not absolutely dependent on presence of epistasis, but it is usually assumed that interactions of nonallelic genes will be a significant feature of any multiple peak system of genotypes. On this assumption WRIGHT’S hypothesis suggests that a population obtained from random crossing among selected clones of an asexual species should exhibit (1) relatively large amounts of genetic variances, and (2) considerable epistatic variance. This manuscript reports and discusses evidence on the genetic variance THE evolutionary forces. These forces are shaped in part by the reproductive sys