Parallel Evolutionary Changes Research Articles

Dynamics of genomic change during evolutionary rescue in the seed beetle Callosobruchus maculatus.

Rapid adaptation can prevent extinction when populations are exposed to extremely marginal or stressful environments. Factors that affect the likelihood of evolutionary rescue from extinction have been identified, but much less is known about the evolutionary dynamics (e.g., rates and patterns of allele frequency change) and genomic basis of successful rescue, particularly in multicellular organisms. We conducted an evolve-and-resequence experiment to investigate the dynamics of evolutionary rescue at the genetic level in the cowpea seed beetle, Callosobruchus maculatus, when it is experimentally shifted to a stressful host plant, lentil. Low survival (~1%) at the onset of the experiment caused population decline. But adaptive evolution quickly rescued the population, with survival rates climbing to 69% by the F5 generation and 90% by the F10 generation. Population genomic data showed that rescue likely was caused by rapid evolutionary change at multiple loci, with many alleles fixing or nearly fixing within five generations of selection on lentil. Selection on these loci was only moderately consistent in time, but parallel evolutionary changes were evident in sublines formed after the lentil line had passed through a bottleneck. By comparing estimates of selection and genomic change on lentil across five independent C. maculatus lines (the new lentil-adapted line, three long-established lines and one case of failed evolutionary rescue), we found that adaptation on lentil occurred via somewhat idiosyncratic evolutionary changes. Overall, our results suggest that evolutionary rescue in this system can be caused by very strong selection on multiple loci driving rapid and pronounced genomic change.

Identifying Drivers of Parallel Evolution: A Regression Model Approach.

Parallel evolution, defined as identical changes arising in independent populations, is often attributed to similar selective pressures favoring the fixation of identical genetic changes. However, some level of parallel evolution is also expected if mutation rates are heterogeneous across regions of the genome. Theory suggests that mutation and selection can have equal impacts on patterns of parallel evolution; however, empirical studies have yet to jointly quantify the importance of these two processes. Here, we introduce several statistical models to examine the contributions of mutation and selection heterogeneity to shaping parallel evolutionary changes at the gene-level. Using this framework, we analyze published data from forty experimentally evolved Saccharomyces cerevisiae populations. We can partition the effects of a number of genomic variables into those affecting patterns of parallel evolution via effects on the rate of arising mutations, and those affecting the retention versus loss of the arising mutations (i.e., selection). Our results suggest that gene-to-gene heterogeneity in both mutation and selection, associated with gene length, recombination rate, and number of protein domains drive parallel evolution at both synonymous and nonsynonymous sites. While there are still a number of parallel changes that are not well described, we show that allowing for heterogeneous rates of mutation and selection can provide improved predictions of the prevalence and degree of parallel evolution.

Comparative Genomics of the Sigatoka Disease Complex on Banana Suggests a Link between Parallel Evolutionary Changes in Pseudocercospora fijiensis and Pseudocercospora eumusae and Increased Virulence on the Banana Host.

The Sigatoka disease complex, caused by the closely-related Dothideomycete fungi Pseudocercospora musae (yellow sigatoka), Pseudocercospora eumusae (eumusae leaf spot), and Pseudocercospora fijiensis (black sigatoka), is currently the most devastating disease on banana worldwide. The three species emerged on bananas from a recent common ancestor and show clear differences in virulence, with P. eumusae and P. fijiensis considered the most aggressive. In order to understand the genomic modifications associated with shifts in the species virulence spectra after speciation, and to identify their pathogenic core that can be exploited in disease management programs, we have sequenced and analyzed the genomes of P. eumusae and P. musae and compared them with the available genome sequence of P. fijiensis. Comparative analysis of genome architectures revealed significant differences in genome size, mainly due to different rates of LTR retrotransposon proliferation. Still, gene counts remained relatively equal and in the range of other Dothideomycetes. Phylogenetic reconstruction based on a set of 46 conserved single-copy genes strongly supported an earlier evolutionary radiation of P. fijiensis from P. musae and P. eumusae. However, pairwise analyses of gene content indicated that the more virulent P. eumusae and P. fijiensis share complementary patterns of expansions and contractions in core gene families related to metabolism and enzymatic degradation of plant cell walls, suggesting that the evolution of virulence in these two pathogens has, to some extent, been facilitated by convergent changes in metabolic pathways associated with nutrient acquisition and assimilation. In spite of their common ancestry and shared host-specificity, the three species retain fairly dissimilar repertoires of effector proteins, suggesting that they likely evolved different strategies for manipulating the host immune system. Finally, 234 gene families, including seven putative effectors, were exclusively present in the three Sigatoka species, and could thus be related to adaptation to the banana host.

The effect of selection environment on the probability of parallel evolution.

Across the great diversity of life, there are many compelling examples of parallel and convergent evolution-similar evolutionary changes arising in independently evolving populations. Parallel evolution is often taken to be strong evidence of adaptation occurring in populations that are highly constrained in their genetic variation. Theoretical models suggest a few potential factors driving the probability of parallel evolution, but experimental tests are needed. In this study, we quantify the degree of parallel evolution in 15 replicate populations of Pseudomonas fluorescens evolved in five different environments that varied in resource type and arrangement. We identified repeat changes across multiple levels of biological organization from phenotype, to gene, to nucleotide, and tested the impact of 1) selection environment, 2) the degree of adaptation, and 3) the degree of heterogeneity in the environment on the degree of parallel evolution at the gene-level. We saw, as expected, that parallel evolution occurred more often between populations evolved in the same environment; however, the extent of parallel evolution varied widely. The degree of adaptation did not significantly explain variation in the extent of parallelism in our system but number of available beneficial mutations correlated negatively with parallel evolution. In addition, degree of parallel evolution was significantly higher in populations evolved in a spatially structured, multiresource environment, suggesting that environmental heterogeneity may be an important factor constraining adaptation. Overall, our results stress the importance of environment in driving parallel evolutionary changes and point to a number of avenues for future work for understanding when evolution is predictable.

Parallel evolution of tetrodotoxin resistance in three voltage-gated sodium channel genes in the garter snake Thamnophis sirtalis.

Members of a gene family expressed in a single species often experience common selection pressures. Consequently, the molecular basis of complex adaptations may be expected to involve parallel evolutionary changes in multiple paralogs. Here, we use bacterial artificial chromosome library scans to investigate the evolution of the voltage-gated sodium channel (Nav) family in the garter snake Thamnophis sirtalis, a predator of highly toxic Taricha newts. Newts possess tetrodotoxin (TTX), which blocks Nav’s, arresting action potentials in nerves and muscle. Some Thamnophis populations have evolved resistance to extremely high levels of TTX. Previous work has identified amino acid sites in the skeletal muscle sodium channel Nav1.4 that confer resistance to TTX and vary across populations. We identify parallel evolution of TTX resistance in two additional Nav paralogs, Nav1.6 and 1.7, which are known to be expressed in the peripheral nervous system and should thus be exposed to ingested TTX. Each paralog contains at least one TTX-resistant substitution identical to a substitution previously identified in Nav1.4. These sites are fixed across populations, suggesting that the resistant peripheral nerves antedate resistant muscle. In contrast, three sodium channels expressed solely in the central nervous system (Nav1.1–1.3) showed no evidence of TTX resistance, consistent with protection from toxins by the blood–brain barrier. We also report the exon–intron structure of six Nav paralogs, the first such analysis for snake genes. Our results demonstrate that the molecular basis of adaptation may be both repeatable across members of a gene family and predictable based on functional considerations.

Multihost experimental evolution of the pathogen Ralstonia solanacearum unveils genes involved in adaptation to plants.

Ralstonia solanacearum, the causal agent of a lethal bacterial wilt plant disease, infects an unusually wide range of hosts. These hosts can further be split into plants where R. solanacearum is known to cause disease (original hosts) and those where this bacterium can grow asymptomatically (distant hosts). Moreover, this pathogen is able to adapt to many plants as supported by field observations reporting emergence of strains with enlarged pathogenic properties. To investigate the genetic bases of host adaptation, we conducted evolution experiments by serial passages of a single clone of the pathogen on three original and two distant hosts over 300 bacterial generations and then analyzed the whole-genome of nine evolved clones. Phenotypic analysis of the evolved clones showed that the pathogen can increase its fitness on both original and distant hosts although the magnitude of fitness increase was greater on distant hosts. Only few genomic modifications were detected in evolved clones compared with the ancestor but parallel evolutionary changes in two genes were observed in independent evolved populations. Independent mutations in the regulatory gene efpR were selected for in three populations evolved on beans, a distant host. Reverse genetic approaches confirmed that these mutations were associated with fitness gain on bean plants. This work provides a first step toward understanding the within-host evolutionary dynamics of R. solanacearum during infection and identifying bacterial genes subjected to in planta selection. The discovery of EfpR as a determinant conditioning host adaptation of the pathogen illustrates how experimental evolution coupled with whole-genome sequencing is a potent tool to identify novel molecular players involved in central life-history traits.

Sexual dimorphism and polymorphism in a Callovian Phlycticeras (Ammonoidea) assemblage of Kutch, India

An assemblage of Phlycticeras Hyatt from a precisely dated zone of Middle Callovian in Kutch, India has been analyzed. Systematic study reveals that this sample can be divided into two size groups. The larger set shows different adult modifications leading to ornamental polymorphism. Polymorphs are very similar, if not identical, to different chronospecies of Europe, which range between Middle to Upper Callovian. They are grouped under well-known Phlycticeras polygonium (Zieten). The group of smaller specimens on the other hand, strongly resembles a species, which has been previously described as Phlycticeras schaumburgi (Waagen) from the younger Upper Callovian horizons in Kutch. It has a peculiar ‘rooster’–like septicarinate keel in the venter near adult aperture. Phlycticeras-Oecoptychius have been considered as a possible dimorphic pair since long, but here shown to have many inconsistencies to support these views. Instead, sexual dimorphism is explored within Phlycticeras and P. polygonium-P. schaumburgi is proposed as possible antidimorphs. A similar association is found in different stratigraphic assemblages of Europe. Interestingly these two morphs show parallel evolutionary changes within the Phlycticeras genus.

Morphological changes in pedal phalanges through ornithopod dinosaur evolution: A biomechanical approach

The evolution of ornithopod dinosaurs provides a well-documented example of the transition from digitigrady to subunguligrady. During this transition, the ornithopod pes was drastically altered from the plesiomorphic dinosaurian morphology (four digits, claw-shaped unguals, strongly concavo-convex joints, phalanges longer than wide, excavated collateral ligament fossae, presence of sagittal ridge, and prominent processes for the attachment of tendons) to a more derived condition (tridactyly, modification of the unguals into hooves, phalanges wider and thinner than long, lack of collateral ligament fossae, loss of sagittal ridge and tendon attachment processes, relatively flattened articular surfaces). These changes are particularly noteworthy given the overall conservatism in pedal morphology seen across Dinosauria. But what are the functional consequences of these specific morphological transitions? To study them, we examine a wide range of pedal morphologies in four non-avian dinosaurs and two birds. Our analyses of the external morphology, two-dimensional models (using Finite Element Analysis), and internal bone structure demonstrate that this evolutionary shift was accompanied by a loss of digit mobility and flexibility. In addition, pedal posture was modified to better align the pes with the main direction of the ground reaction force, thus becoming well suited to support high loads. These conclusions can be applied to other, parallel evolutionary changes (in both dinosaurs and mammals) that involved similar transitions to a subunguligrade posture.

Rapid parallel evolutionary changes of gene transcription profiles in farmed Atlantic salmon

Farmed salmon strains have been selected to improve growth rates as well as other traits of commercial interest but the 2 million farmed salmon escaping annually may enhance the risk of extinction of wild populations through genetic and ecological interactions. Here, we compare the transcription profiles of 3557 genes in the progeny of farmed and wild Atlantic salmon from Norway and Canada grown in controlled conditions, and demonstrate that five to seven generations of artificial selection led to heritable changes in gene transcription profiles, the average magnitude of the differences being 25% and 18% for at least 1.4% and 1.7% of the expressed genes in juvenile salmon from Norway and Canada, respectively. Moreover, genes showing significant transcription profile differences in both farmed strains (16%) all exhibited parallel changes. These findings, along with the identification of several genes whose expression profiles were modified through artificial selection, provide new insights into the molecular basis of parallel evolution, and suggest how gene flow from farmed escapees may affect the genetic integrity of wild populations.

Allelic Melanism in American and British Peppered Moths

Parallel evolutionary changes in the incidence of melanism are well documented in widely geographically separated subspecies of the peppered moth (Biston betularia). The British melanic phenotype (f. carbonaria) and the American melanic phenotype (f. swettaria) are indistinguishable in appearance, and previous genetic analysis has established that both are inherited as autosomal dominants. This report demonstrates through hybridizations of the subspecies and Mendelian testcrosses of melanic progeny that carbonaria and swettaria are phenotypes produced by alleles (isoalleles) at a single locus. The possibility of close linkage at two loci remains, but the simpler one-locus model cannot be rejected in the absence of contrary evidence.

Origins of Modern Races of Mankind

SIR ARTHUR KEITH'S presidential address to the first Speleological Conference of the British Speleological Association held at Buxton on July 25 made a bold attempt to resolve a number-of doubts and difficulties, which arise out of recent developments in the study of human palaeontology. This, Sir Arthur was careful to point out, is a matter relevant to the purpose of the Conference in that discoveries of the remains of ancient types of man in caves have provided a great part of the material, which points to the necessity of recasting the current view that modern races, black, white, brown and yellow, evolved from a common mid-Pleistocene ancestral stock. It will be remembered that it has been demonstrated recently (see NATURE, 137, 73; 1936) that certain characteristics of the modern Mongolian are to be observed in the remains of Peking man found in the cave of Chou Kou Tien. Sir Arthur would go further. Not only does he too find resemblances to the Mongolian in Peking man, but he also observes Australian and Negro characteristics in Pithecanthropus from Java and the Kanam skull from East Africa respectively. From this evidence, therefore, he draws, somewhat tentatively, the conclusion that at the beginning of the Pleistocene, the ancestors of the Mongol, the Australian and the Negro were already in occupation of the continental areas now inhabited by their descendants; and that after their separation each race underwent a series of parallel evolutionary changes in teeth, jaws, brain and other features showing simian affinities.