Evolution’s past and future: an introduction and partial précis to Stephen Jay Gould’s The Structure of Evolutionary Theory

In The Structure of Evolutionary Theory, his last and largest book on evolution, Stephen Jay Gould conceives of the structure of evolutionary theory since Darwin as comprising three major propositions. First, natural selection is the most important direction-giving force in evolution. Second, it operates at the level of the individual organism. Third, selection can be extrapolated smoothly from its actions on individuals in living species throughout geologic time, to produce the gradual divergence of species and adaptations that characterizes the history of life. Challenges to each of these major propositions, according to Gould, can be of three kinds of severity. The most severe challenges, if true, would nullify one of the major propositions entirely, thus destroying the integration of the theory (and perhaps the logic and support of its other propositions). Other, less severe challenges would revise, modify, and expand the content and scope of one or another of the propositions, but not destroy any of them or the theory in toto. Still other, even less severe challenges add to what is known and extend the scope and possibilities of the theory, but do not call for a revision in its fundamental structure. Gould acknowledges that the theory has withstood all presumptive challenges that would destroy it, and has accommodated those that simply extend and add to it. His principal concern is with those challenges that would revise the theory substantially: for example, if processes other than natural selection were of great importance in evolution; if selection acted in important ways at the level of species and clades, and (or) at the level of the genes, alleles, and chromosomes; and if the extrapolation of what is known from living populations could not by itself explain many patterns of large-scale evolution seen in the fossil record. He thinks that, both through the history of evolution since Darwin and in the present day, challenges that substantially revise these basic propositions are valid, and that the theory needs to integrate them in order to retain the explanatory power that it has had for many decades. To cite this article: K. Padian, C. R. Palevol 2 (2003).     

Cyto‐nuclear discordance suggests complex evolutionary history in the cave‐dwelling salamander,Eurycea lucifuga

Our understanding of the evolutionary history and ecology of cave‐associated species has been driven historically by studies of morphologically adapted cave‐restricted species. Our understanding of the evolutionary history and ecology of nonrestricted cave species, troglophiles, is limited to a few studies, which present differing accounts of troglophiles’ relationship with the cave habitat, and its impact on population dynamics. Here, we used phylogenetics, demographic statistics, and population genetic methods to study lineage divergence, dates of divergence, and population structure in the Cave Salamander, Eurycea lucifuga, across its range. In order to perform these analyses, we sampled 233 individuals from 49 populations, using sequence data from three gene loci as well as genotyping data from 19 newly designed microsatellite markers. We find, as in many other species studied in a phylogeographic context, discordance between patterns inferred from mitochondrial relationships and those inferred by nuclear markers indicating a complicated evolutionary history in this species. Our results suggest Pleistocene‐based divergence among three main lineages within E. lucifuga corresponding to the western, central, and eastern regions of the range, similar to patterns seen in species separated in multiple refugia during climatic shifts. The conflict between mitochondrial and nuclear patterns is consistent with what we would expect from secondary contact between regional populations following expansion from multiple refugia.     

Monomer Abundance Distribution Patterns as a Universal Biosignature: Examples from Terrestrial and Digital Life

Organisms leave a distinctive chemical signature in their environment because they synthesize those molecules that maximize their fitness. As a result, the relative concentrations of related chemical monomers in life-bearing environmental samples reflect, in part, those compounds’ adaptive utility. In contrast, rates of molecular synthesis in a lifeless environment are dictated by reaction kinetics and thermodynamics, so concentrations of related monomers in abiotic samples tend to exhibit specific patterns dominated by small, easily formed, low-formation-energy molecules. We contend that this distinction can serve as a universal biosignature: the measurement of chemical concentration ratios that belie formation kinetics or equilibrium thermodynamics indicates the likely presence of life. We explore the features of this biosignature as observed in amino acids and carboxylic acids, using published data from numerous studies of terrestrial sediments, abiotic (spark, UV, and high-energy proton) synthesis experiments, and meteorite bodies. We then compare these data to the results of experimental studies of an evolving digital life system. We observe the robust and repeatable evolution of an analogous biosignature in a digital lifeform, suggesting that evolutionary selection necessarily constrains organism composition and that the monomer abundance biosignature phenomenon is universal to evolved biosystems.     

How phenotypic convergence arises in experimental evolution

Evolutionary convergence is a core issue in the study of adaptive evolution, as well as a highly debated topic at present. Few studies have analyzed this issue using a “real‐time” or evolutionary trajectory approach. Do populations that are initially differentiated converge to a similar adaptive state when experiencing a common novel environment? Drosophila subobscura populations founded from different locations and years showed initial differences and variation in evolutionary rates in several traits during short‐term (～20 generations) laboratory adaptation. Here, we extend that analysis to 40 more generations to analyze (1) how differences in evolutionary dynamics among populations change between shorter and longer time spans, and (2) whether evolutionary convergence occurs after 60 generations of evolution in a common environment. We found substantial variation in longer term evolutionary trajectories and differences between short‐ and longer term evolutionary dynamics. Although we observed pervasive patterns of convergence toward the character values of long‐established populations, populations still remain differentiated for several traits at the final generations analyzed. This pattern might involve transient divergence, as we report in some cases, indicating that more generations should lead to final convergence. These findings highlight the importance of longer term studies for understanding convergent evolution.     

EXPERIMENTAL EVIDENCE FOR THE EVOLUTION OF THE MAMMALIAN BACULUM BY SEXUAL SELECTION

Male genitalia exhibit a taxonomically widespread pattern of rapid and divergent evolution. Sexual selection is generally believed to be responsible for these patterns of evolutionary divergence, although empirical support for the sexual selection hypothesis comes mainly from studies of insects. Here we show that sexual selection is responsible for an evolutionary divergence in baculum morphology among populations of house mice Mus domesticus. We sourced mice from three isolated populations known to be subject to differing strengths of postcopulatory sexual selection and bred them under common‐garden conditions. Mice from populations with strong postcopulatory sexual selection had bacula that were relatively thicker compared with mice from populations with weak selection. We used experimental evolution to determine whether these patterns of divergence could be ascribed to postcopulatory sexual selection. After 27 generations of experimental evolution, populations of mice subjected to postcopulatory sexual selection evolved bacula that were relatively thicker than populations subjected to enforced monogamy. Our data thereby provide evidence that postcopulatory sexual selection underlies an evolutionary divergence in the mammalian baculum and supports the hypothesis that sexual selection plays a general role in the evolution of male genital morphology across evolutionary diverse taxonomic groups.     

Head shape variation among cryptic populations of ground skinks (Scincella lateralis)

Recent interest in testing the river–refugia effect has prompted an evolutionary investigation of the ground skink (Scincella lateralis) to diagnose instances of the riverine barrier hypothesis and thus, Pleistocene climate change refugia. This taxon, characterized by limited vagility, presents itself as a model organism in understanding patterns in Gulf Coast squamate evolution and biogeography. Here, we use geometric morphometric techniques to assess whether changes in head shape characterize diverging molecular lineages. We analysed head shape variation for diagnostic morphology by population and hypothesized that clades recovered as monophyletic by previous molecular studies will be more similar to each other than distantly related lineages. Dorsal and lateral head shape analyses indicated strong divergence for one clade (mitochondrial Clade I) in association with mtDNA divergence, exhibiting cranial narrowing and elongation relative to all other clades, and weak divergence of another clade (mitochondrial Clade N), which exhibited similar shape divergence from consensus. Both of these clades are Gulf Coast lineages and our results suggest convergence in head shape towards a regional phenotype.     

The predictability of genomic changes underlying a recent host shift in Melissa blue butterflies

Despite accumulating evidence that evolution can be predictable, studies quantifying the predictability of evolution remain rare. Here, we measured the predictability of genome‐wide evolutionary changes associated with a recent host shift in the Melissa blue butterfly (Lycaeides melissa). We asked whether and to what extent genome‐wide patterns of evolutionary change in nature could be predicted (i) by comparisons among instances of repeated evolution and (ii) from SNP × performance associations in a laboratory experiment. We delineated the genetic loci (SNPs) most strongly associated with host use in two L. melissa lineages that colonized alfalfa. Whereas most SNPs were strongly associated with host use in none or one of these lineages, we detected a an approximately twofold excess of SNPs associated with host use in both lineages. Similarly, we found that host‐associated SNPs in nature could also be partially predicted from SNP × performance (survival and weight) associations in a laboratory rearing experiment. But the extent of overlap, and thus degree of predictability, was somewhat reduced. Although we were able to predict (to a modest extent) the SNPs most strongly associated with host use in nature (in terms of parallelism and from the experiment), we had little to no ability to predict the direction of evolutionary change during the colonization of alfalfa. Our results show that different aspects of evolution associated with recent adaptation can be more or less predictable and highlight how stochastic and deterministic processes interact to drive patterns of genome‐wide evolutionary change.     

Morphological and niche divergence of pinyon pines

The environmental variables that define a species ecological niche should be associated with the evolutionary patterns present in the adaptations that resulted from living in these conditions. Thus, when comparing across species, we can expect to find an association between phylogenetically independent phenotypic characters and ecological niche evolution. Few studies have evaluated how organismal phenotypes might mirror patterns of niche evolution if these phenotypes reflect adaptations. Doing so could contribute on the understanding of the origin and maintenance of phenotypic diversity observed in nature. Here, we show the pattern of niche evolution of the pinyon pine lineage (Pinus subsection Cembroides); then, we suggest morphological adaptations possibly related to niche divergence, and finally, we test for correlation between ecological niche and morphology. We demonstrate that niche divergence is the general pattern within the clade and that it is positively correlated with adaptation.     

Sex‐biased transcriptome divergence along a latitudinal gradient

Sex‐dependent gene expression is likely an important genomic mechanism that allows sex‐specific adaptation to environmental changes. Among Drosophila species, sex‐biased genes display remarkably consistent evolutionary patterns; male‐biased genes evolve faster than unbiased genes in both coding sequence and expression level, suggesting sex differences in selection through time. However, comparatively little is known of the evolutionary process shaping sex‐biased expression within species. Latitudinal clines offer an opportunity to examine how changes in key ecological parameters also influence sex‐specific selection and the evolution of sex‐biased gene expression. We assayed male and female gene expression in Drosophila serrata along a latitudinal gradient in eastern Australia spanning most of its endemic distribution. Analysis of 11 631 genes across eight populations revealed strong sex differences in the frequency, mode and strength of divergence. Divergence was far stronger in males than females and while latitudinal clines were evident in both sexes, male divergence was often population specific, suggesting responses to localized selection pressures that do not covary predictably with latitude. While divergence was enriched for male‐biased genes, there was no overrepresentation of X‐linked genes in males. By contrast, X‐linked divergence was elevated in females, especially for female‐biased genes. Many genes that diverged in D. serrata have homologs also showing latitudinal divergence in Drosophila simulans and Drosophila melanogaster on other continents, likely indicating parallel adaptation in these distantly related species. Our results suggest that sex differences in selection play an important role in shaping the evolution of gene expression over macro‐ and micro‐ecological spatial scales.     

Phenotypic plasticity and divergence in gene expression

The extent to which phenotypic plasticity, or the ability of a single genotype to produce different phenotypes in different environments, impedes or promotes genetic divergence has been a matter of debate within evolutionary biology for many decades (see, for example, Ghalambor et al. 2007 ; Pfennig et al. 2010 ). Similarly, the role of evolution in shaping phenotypic plasticity remains poorly understood (Pigliucci 2005 ). In this issue of Molecular Ecology, Dayan et al. ( 2015 ) provide empirical data relevant to these questions by assessing the extent of plasticity and divergence in the expression levels of 2272 genes in muscle tissue from killifish (genus Fundulus) exposed to different temperatures. F. heteroclitus (Fig.  1 A) and F. grandis are minnows that inhabit estuarine marshes (Fig.  1 B) along the coasts of the Atlantic Ocean and Gulf of Mexico in North America. These habitats undergo large variations in temperature both daily and seasonally, and these fish are known to demonstrate substantial phenotypic plasticity in response to temperature change (e.g. Fangue et al. 2006 ). Furthermore, the range of F. heteroclitus spans a large latitudinal gradient of temperatures, such that northern populations experience temperatures that are on average ~10°C colder than do southern populations (Schulte 2007 ). By comparing gene expression patterns between populations of these fish from different thermal habitats held in the laboratory at three different temperatures, Dayan et al. ( 2015 ) address two important questions regarding the interacting effects of plasticity and evolution: (i) How does phenotypic plasticity affect adaptive divergence? and (ii) How does adaptive divergence affect plasticity?     

Multiple Facets of Exploratory Behavior in House Crickets (Acheta domesticus): Split Personalities or Simply Different Behaviors?

Behavioral ecologists are increasingly interested in patterns of repeatable variation in behaviors. The study of this variation, under the label ‘animal personality’, frequently makes assumptions both in regards to what the ecological significance of particular behavioral responses might be and whether different methodologies in fact test the same behavior. Here, using house crickets (Acheta domesticus), we tested whether stereotypical approaches to quantifying repeatable variation in exploratory behavior measured the same behaviors. We found that house cricket exploratory behavior was highly repeatable in two populations (repeatability: 0.37–0.51). However, exploratory behavior across two different testing methods was not strongly correlated (r = ?0.17 to 0.14). This suggests that either different behaviors or distinct components of exploratory behavior were being measured. Our results also support recent criticisms that care needs to be taken in describing personality traits.     

Molecular Phylogeny of the Family Ophryscolecidae (Ciliophora,Litostomatea) Inferred from 18S rDNA Sequences

The 18S rDNA was used to infer oral ciliature patterns of evolution within the family Ophryoscolecidae, with the addition of five new sequences of ciliates from the genus Ostracodinium. Our data confirmed the monophyly of the subfamilies Entodiniinae and Ophryoscolecinae, but more analysis would be required for the definition of the status of the subfamily Diplodiniinae. The oral infraciliature patterns reflect evolutionary divergence in the family Ophryscolecidae, observing monophyly on Entodinium‐type, Diplodinium‐type, Ostracodinium‐type, Epidinium‐type, and Ophryoscolex‐type. The ancestral infraciliature of Entodinium‐type cannot be proven, however, the position of Entodinium‐type showed closer of Diplodinium‐type than Ophryoscolex‐type, corroborating previous studies using morphological characters. The observed inconsistencies reflect the need to increase the number of 18S rDNA sequences to family Ophryoscolecidae and investigate the evolution of this group using other molecular markers.     

Testing alternative hypotheses for evolutionary diversification in an African songbird: rainforest refugia versus ecological gradients

Geographic isolation in rainforest refugia and local adaptation to ecological gradients may both be important drivers of evolutionary diversification. However, their relative importance and the underlying mechanisms of these processes remain poorly understood because few empirical studies address both putative processes in a single system. A key question is to what extent is divergence in signals that are important in mate and species recognition driven by isolation in rainforest refugia or by divergent selection across ecological gradients? We studied the little greenbul, Andropadus virens, an African songbird, in Cameroon and Uganda, to determine whether refugial isolation or ecological gradients better explain existing song variation. We then tested whether song variation attributable to refugial or ecological divergence was biologically meaningful using reciprocal playback experiments to territorial males. We found that much of the existing song variation can be explained by both geographic isolation and ecological gradients, but that divergence across the gradient, and not geographic isolation, affects male response levels. These data suggest that ecologically divergent traits, independent of historical isolation during glacial cycles, can promote reproductive isolation. Our study provides further support for the importance of ecology in explaining patterns of evolutionary diversification in ecologically diverse regions of the planet.     

Correlated patterns of genetic diversity and differentiation across an avian family

Comparative studies of closely related taxa can provide insights into the evolutionary forces that shape genome evolution and the prevalence of convergent molecular evolution. We investigated patterns of genetic diversity and differentiation in stonechats (genus Saxicola), a widely distributed avian species complex with phenotypic variation in plumage, morphology and migratory behaviour, to ask whether similar genomic regions have become differentiated in independent, but closely related, taxa. We used whole‐genome pooled sequencing of 262 individuals from five taxa and found that levels of genetic diversity and divergence are strongly correlated among different stonechat taxa. We then asked whether these patterns remain correlated at deeper evolutionary scales and found that homologous genomic regions have become differentiated in stonechats and the closely related Ficedula flycatchers. Such correlation across a range of evolutionary divergence and among phylogenetically independent comparisons suggests that similar processes may be driving the differentiation of these independently evolving lineages, which in turn may be the result of intrinsic properties of particular genomic regions (e.g. areas of low recombination). Consequently, studies employing genome scans to search for areas important for reproductive isolation or adaptation should account for corresponding regions of differentiation, as these regions may not necessarily represent speciation islands or evidence of local adaptation.     

Do Correlation Patterns Reflect the Role of Development in Morphological Evolution?

Correlation patterns have been widely used in evolutionary studies for exploring the role of development in channelling morphological evolution. The approach was firstly introduced by Olson and Miller in the 1950s, but it did not gain prominence until the 1980s, due to some extent to Gould and Lewontin’s (Proc R Soc Lond B 205:581–598, 1979) assertion of the importance of considering organisms as integrated entities, where the internal organization of a structure, and not only the selective regime acting upon it, would play a fundamental role in its evolution. Here we show that this approach, mainly focused on the study of small, quantitative shape changes of existing structures, does not deal with a fundamental aspect of developmental systems, that is, their intrinsic capacity of originating morphological novelties. We show that only when the physicochemical processes underlying morphogenesis and pattern formation are taken into account, would the causal role of development be fully incorporated into the evolutionary view.     

Rapid divergence and convergence of life‐history in experimentally evolved Drosophila melanogaster

Laboratory selection experiments are alluring in their simplicity, power, and ability to inform us about how evolution works. A longstanding challenge facing evolution experiments with metazoans is that significant generational turnover takes a long time. In this work, we present data from a unique system of experimentally evolved laboratory populations of Drosophila melanogaster that have experienced three distinct life‐history selection regimes. The goal of our study was to determine how quickly populations of a certain selection regime diverge phenotypically from their ancestors, and how quickly they converge with independently derived populations that share a selection regime. Our results indicate that phenotypic divergence from an ancestral population occurs rapidly, within dozens of generations, regardless of that population's evolutionary history. Similarly, populations sharing a selection treatment converge on common phenotypes in this same time frame, regardless of selection pressures those populations may have experienced in the past. These patterns of convergence and divergence emerged much faster than expected, suggesting that intermediate evolutionary history has transient effects in this system. The results we draw from this system are applicable to other experimental evolution projects, and suggest that many relevant questions can be sufficiently tested on shorter timescales than previously thought.