PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY

The problem of complex adaptations is studied in two largely disconnected research traditions: evolutionary biology and evolutionary computer science. This paper summarizes the results from both areas and compares their implications. In evolutionary computer science it was found that the Darwinian process of mutation, recombination and selection is not universally effective in improving complex systems like computer programs or chip designs. For adaptation to occur, these systems must possess “evolvability,” i.e., the ability of random variations to sometimes produce improvement. It was found that evolvability critically depends on the way genetic variation maps onto phenotypic variation, an issue known as the representation problem. The genotype-phenotype map determines the variability of characters, which is the propensity to vary. Variability needs to be distinguished from variations, which are the actually realized differences between individuals. The genotype-phenotype map is the common theme underlying such varied biological phenomena as genetic canalization, developmental constraints, biological versatility, developmental dissociability, and morphological integration. For evolutionary biology the representation problem has important implications: how is it that extant species acquired a genotype-phenotype map which allows improvement by mutation and selection? Is the genotype-phenotype map able to change in evolution? What are the selective forces, if any, that shape the genotype-phenotype map? We propose that the genotype-phenotype map can evolve by two main routes: epistatic mutations, or the creation of new genes. A common result for organismic design is modularity. By modularity we mean a genotype-phenotype map in which there are few pleiotropic effects among characters serving different functions, with pleiotropic effects falling mainly among characters that are part of a single functional complex. Such a design is expected to improve evolvability by limiting the interference between the adaptation of different functions. Several population genetic models are reviewed that are intended to explain the evolutionary origin of a modular design. While our current knowledge is insufficient to assess the plausibility of these models, they form the beginning of a framework for understanding the evolution of the genotype-phenotype map.     

DECIPHERING THE EVOLUTIONARY HISTORY AND DEVELOPMENTAL MECHANISMS OF A COMPLEX SEXUAL ORNAMENT: THE ABDOMINAL APPENDAGES OF SEPSIDAE (DIPTERA)

Male abdomen appendages are a novel trait found within Sepsidae (Diptera). Here we demonstrate that they are likely to have evolved once, were lost three times, and then secondarily gained in one lineage. The developmental basis of these appendages was investigated by counting the number of histoblast cells in each abdominal segment in four species: two that represented the initial instance of appendage evolution, one that has secondarily gained appendages, and one species that did not have appendages. Males of all species with appendages have elevated cell counts for the fourth segment, which gives rise to the appendages. In Perochaeta dikowi, which reacquired the trait, the females also have elevated cell count on the fourth segment despite the fact that females do not develop appendages. The species without appendages has similar cell counts in all segments regardless of sex. These results suggest that the basis for appendage development is shared in males across all species, but the sexual dimorphism is regulated differently in P. dikowi.     

论紫堇属的系统演化与区系发生和区系分区的关系

紫堇属ＣｏｒｙｄａｌｉｓＤＣ．是紫堇科Ｆｕｍａｒｉｃａｅａｅ的最大属,也是北温带分布型的大属之一。本属自建立以来,迄今尚无完整的分类系统,甚至连属的命名人,后造属模式以及属下分类单位的划分均存在许多争议,本文根据作者们二十多年来在国内外有关标本室收集的模式标本和有关东亚,南亚标本,经过鉴定整理,首次将本属划分为两大类群,即Ｃｒｏｙｄａｌｉｓ群和Ｐｉｓｔｏｌｃｈｉａ群和４０个组,并初步建立了一个较全     

小麦的穗领在系统演化和个体发育中形成过程的初步探讨

小麦的穗领有三种类型:领腹完全敞开的U形穗领、领腹完全闭合的O形穗领和领腹呈V型交叉的V形穗领。穗领是系统演化中顶生叶叶鞘减化后的遗迹,也是个体发育中穗轴基部第一侧生小穗下苞叶原始体的痕迹。在一定条件下,从穗领可以长出叶鞘和叶片,穗轴基部节间可以变为茎节间,穗领腋内的小穗可以变为腋芽、带柄分枝穗或分枝花序。其余侧生小穗下都有一个领腹完全敞开的U形小穗领,其形态与U形穗领相似。它们是系统演化中二次轴分枝花序的苞叶叶鞘减化后的遗迹,也是个体发育中苞原始体的痕迹。一定条件下,从小穗领也可以长出叶鞘和叶片。穗轴基部节间变茎的同时,基部几个小穗若发生向圆锥花序的部分返祖变异,随着变异程度加深,从穗领和小穗领逐渐形成叶鞘和叶片。说明在系统演化中。顶生叶和苞叶先减化叶片,后减化叶鞘,最后形成穗领和小穗领。小麦祖先的花序与茎叶之间没有明显的界限。     

FISHER'S MODEL AND THE GENOMICS OF ADAPTATION: RESTRICTED PLEIOTROPY,HETEROGENOUS MUTATION,AND PARALLEL EVOLUTION

Genetic theories of adaptation generally overlook the genes in which beneficial substitutions occur, and the likely variation in their mutational effects. We investigate the consequences of heterogeneous mutational effects among loci on the genetics of adaptation. We use a generalization of Fisher's geometrical model, which assumes multivariate Gaussian stabilizing selection on multiple characters. In our model, mutation has a distinct variance–covariance matrix of phenotypic effects for each locus. Consequently, the distribution of selection coefficients s varies across loci. We assume each locus can only affect a limited number of independent linear combinations of phenotypic traits (restricted pleiotropy), which differ among loci, an effect we term “orientation heterogeneity.” Restricted pleiotropy can sharply reduce the overall proportion of beneficial mutations. Orientation heterogeneity has little impact on the shape of the genomic distribution, but can substantially increase the probability of parallel evolution (the repeated fixation of beneficial mutations at the same gene in independent populations), which is highest with low pleiotropy. We also consider variation in the degree of pleiotropy and in the mean s across loci. The latter impacts the genomic distribution of s, but has a much milder effect on parallel evolution. We discuss these results in the light of evolution experiments.     

A PHYLOGENETIC APPROACH TO THE ESTIMATION OF PHYTOPLANKTON TRAITS1

The quantitative characterization of the ecology of individual phytoplankton taxa is essential for model resolution of many aspects of aquatic ecosystems. Existing literature cannot directly parameterize all phytoplankton taxa of interest, as many traits and taxa have not been sampled. However, valuable clues on the value of traits are found in the evolutionary history of species and in common correlations between traits. These two resources were exploited with an existing, statistically consistent method built upon evolutionary concepts. From a new data set with >700 observations on freshwater phytoplankton traits and a qualitative phytoplankton phylogeny, estimates were derived for the size, growth rate, phosphate affinity, and susceptibility to predation of 277 phytoplankton types, from evolutionary ancestors to present‐day species. These estimates account simultaneously for phylogenetic relationships between types, as imposed by the phylogeny, and approximate power‐law relationships (e.g., allometric scaling laws) between traits, as reconstructed from the data set. Results suggest that most phytoplankton traits are to some extent conserved in evolution: cross‐validation demonstrated that the use of phylogenetic information significantly improves trait value estimates. By providing trait value estimates as well as uncertainties, these results could benefit most quantitative studies involving phytoplankton.     

DEVELOPMENTAL STABILITY IN LEAVES OF CLARKIA TEMBLORIENSIS (ONAGRACEAE) AS RELATED TO POPULATION OUTCROSSING RATES AND HETEROZYGOSITY

Four natural populations of Clarkia tembloriensis, whose levels of heterozygosity and rates of outcrossing were previously found to be correlated, are examined for developmental instability in their leaves. From the northern end of the species range, we compare a predominantly selfing population (t? = 0.26) with a more outcrossed population (t? = 0.84), which is genetically similar. From the southern end of the range, we compare a highly selfing population (t? = 0.03) with a more outcrossed population (t? = 0.58). We measured developmental stability in the populations using two measures of within-plant variation in leaf length as well as calculations of fluctuating asymmetry (FA) for several leaf traits. Growth-chamber experiments show that selfing populations are significantly more variable in leaf length than more outcrossed populations. Developmental instability can contribute to this difference in population-level variance. Plants from more homozygous populations tend to have greater within-plant variance over developmentally comparable nodes than plants from more heterozygous populations, but the difference is not significant. At the upper nodes of the plant, mature leaf length declines steadily with plant age, allowing for a regression of leaf length on node. On average, the plants from more homozygous populations showed higher variance about the regression (MSE) and lower R² values, suggesting that the decline in leaf length with plant age is less stable in plants from selfing populations than in plants from outcrossing populations. Fluctuating asymmetry (FA) was calculated for four traits within single leaves at up to five nodes per plant. At the early nodes of the plant where leaf arrangement is opposite, FA was also calculated for the same traits between opposite leaves at a node. Fluctuating asymmetry is significantly greater in the southern selfing population than in the neighboring outcrossed population. Northern populations do not differ in FA. Fluctuating asymmetry can vary significantly between nodes. The FA values of different leaf traits were not correlated. We show that developmental stability can be measured in plants using FA and within-plant variance. Our data suggest that large differences in breeding system are associated with differences in stability, with more inbred populations being the least stable.     

DISENTANGLING THE CONTRIBUTION OF SEXUAL SELECTION AND ECOLOGY TO THE EVOLUTION OF SIZE DIMORPHISM IN PINNIPEDS

The positive relationship between sexual size dimorphism (SSD) and harem size across pinnipeds is often cited as a textbook example of sexual selection. It assumes that female aggregation selected for large male size via male–male competition. Yet, it is also conceivable that SSD evolved prior to polygyny due to ecological forces. We analyzed 11 life‐history traits in 35 pinniped species to determine their coevolutionary dynamics and infer their most likely evolutionary trajectories contrasting these two hypotheses. We find support for SSD having evolved prior to changes in the mating system, either as a consequence of niche partitioning during aquatic foraging or in combination with sexual selection on males to enforce copulations on females. Only subsequently did polygyny evolve, leading to further coevolution as the strength of sexual selection intensified. Evolutionary sequence analyses suggest a polar origin of pinnipeds and indicate that SSD and polygyny are intrinsically linked to a suite of ecological and life‐history traits. Overall, this study calls for the inclusion of ecological variables when studying sexual selection and argues for caution when assuming causality between coevolving traits. It provides novel insights into the role of sexual selection for the coevolutionary dynamics of SSD and mating system.     

THE EVOLUTION OF CANALIZATION AND THE BREAKING OF VON BAER'S LAWS: MODELING THE EVOLUTION OF DEVELOPMENT WITH EPISTASIS

Evolution can change the developmental processes underlying a character without changing the average expression of the character itself. This sort of change must occur in both the evolution of canalization, in which a character becomes increasingly buffered against genetic or developmental variation, and in the phenomenon of closely related species that show similar adult phenotypes but different underlying developmental patterns. To study such phenomena, I develop a model that follows evolution on a surface representing adult phenotype as a function of underlying developmental characters. A contour on such a “phenotype landscape” is a set of states of developmental characters that produce the same adult phenotype. Epistasis induces curvature of this surface, and degree of canalization is represented by the slope along a contour. I first discuss the geometric properties of phenotype landscapes, relating epistasis to canalization. I then impose a fitness function on the phenotype and model evolution of developmental characters as a function of the fitness function and the local geometry of the surface. This model shows how canalization evolves as a population approaches an optimum phenotype. It further shows that under some circumstances, “decanalization” can occur, in which the expression of adult phenotype becomes increasingly sensitive to developmental variation. This process can cause very similar populations to diverge from one another developmentally even when their adult phenotypes experience identical selection regimes.     

ARTIFICIAL SELECTION FOR DEVELOPMENTAL TIME IN DROSOPHILA MELANOGASTER IN RELATION TO THE EVOLUTION OF AGING: DIRECT AND CORRELATED RESPONSES

A wild-type strain of Drosophila melanogaster was successfully selected for both fast and slow larval development. The realized heritabilities (h²) ranged from 0.20 to 0.30 for the fast lines and 0.35 to 0.60 for the slow lines. The selection applied is relevant in relation to the evolution of aging. The longevity of adults, either virgin or mated, was not affected by selection for developmental time, indicating that developmental time is not a causal determinant of life span, thus confirming the results of the studies on environmental effects on aging (Zwaan et al. 1991, 1992). However, adult body weights were higher in the slow developmental lines and lower in the fast lines, relative to the control flies. Furthermore, slow females showed relatively high early fecundity and low late fecundity, as compared with control and fast females. Mated longevities and total lifetime progeny productions were not statistically different. Previous results obtained by other authors from selection experiments on age at reproduction either supported the mutation accumulation or the negative pleiotropy theory of aging (Luckinbill et al. 1984; Rose 1984b). The impact of the reported results on the interpretation of these studies is discussed, and it is noted that direct selection on adult longevity is needed to settle this issue.     

THE EVOLUTION OF DEVELOPMENT IN DROSOPHILA MELANOGASTER SELECTED FOR POSTPONED SENESCENCE

The role of development in the evolution of postponed senescence is poorly understood despite the existence of a major gerontological theory connecting developmental rate to aging. We investigate the role of developmental rate in the laboratory evolution of aging using 24 distinct populations of Drosophila melanogaster. We have found a significant difference between the larval developmental rates of our Drosophila stocks selected for early (B) and late-life (O) fertility. This larval developmental time difference of approximately 12% (O > B) has been stable for at least 5 yr, occurs under a wide variety of rearing conditions, responds to reverse selection, and is shown for two other O-like selection treatments. Emerging adults from lines with different larval developmental rates show no significant differences in weight at emergence, thorax length, or starvation resistance. Long-developing lines (O, CO, and CB) have greater survivorship from egg to pupa and from pupa to adult, with and without strong larval competition. Crosses between slower developing populations, and a variety of other lines of evidence, indicate that neither mutation accumulation nor inbreeding depression are responsible for the extended development of our late-reproduced selection treatments. These results stand in striking contrast to other recent studies. We argue that inbreeding depression and inadvertent direct selection in other laboratories' culture regimes explain their results. We demonstrate antagonistic pleiotropy between developmental rate and preadult viability. The absence of any correlation between longevity and developmental time in our stocks refutes the developmental theory of aging.     

HOW LIZARDS TURN INTO SNAKES: A PHYLOGENETIC ANALYSIS OF BODY-FORM EVOLUTION IN ANGUID LIZARDS

Abstract One of the most striking morphological transformations in vertebrate evolution is the transition from a lizardlike body form to an elongate, limbless (snakelike) body form. Despite its dramatic nature, this transition has occurred repeatedly among closely related species (especially in squamate reptiles), making it an excellent system for studying macroevolutionary transformations in body plan. In this paper, we examine the evolution of body form in the lizard family Anguidae, a clade in which multiple independent losses of limbs have occurred. We combine a molecular phylogeny for 27 species, our morphometric data, and phylogenetic comparative methods to provide the first statistical phylogenetic tests of several long‐standing hypotheses for the evolution of snakelike body form. Our results confirm the hypothesized relationships between body elongation and limb reduction and between limb reduction and digit reduction. However, we find no support for the hypothesized sequence going from body elongation to limb reduction to digit loss, and we show that a burrowing lifestyle is not a necessary correlate of limb loss. We also show that similar degrees of overall body elongation are achieved in two different ways in anguids, that these different modes of elongation are associated with different habitat preferences, and that this dichotomy in body plan and ecology is widespread in limb‐reduced squamates. Finally, a recent developmental study has proposed that the transition from lizardlike to snakelike body form involves changes in the expression domains of midbody Hox genes, changes that would link elongation and limb loss and might cause sudden transformations in body form. Our results reject this developmental model and suggest that this transition involves gradual changes occurring over relatively long time scales.     

DATA AND DATA INTERPRETATION IN THE STUDY OF LIMB EVOLUTION: A REPLY TO GALIS ET AL. ON THE REEVOLUTION OF DIGITS IN THE LIZARD GENUS BACHIA

Galis and collaborators (2010) claim that our recent paper ( Kohlsdorf and Wagner 2006 ), presenting statistical evidence for the reevolution of digits in the genus Bachia, may be flawed. Their reanalysis of the data does not support the possibility of a reevolution of digits and the authors also argue that such a reevolution would be implausible on functional and developmental grounds. In response, we reanalyzed our data with additional outgroup species. Our results differ from the one published in 2006, but this incongruence is not statistically significant. In contrast, the hypothesis presented by Galis et al. is significantly worse. An analysis of digit number evolution, using novel techniques to test for irreversibility of character loss ( Goldberg and Igic 2008 ), confirmed our original conclusion that there is strong evidence for reevolution of digits in Bachia. We also point out that this result is not in conflict with the hypothesis by Galis and Metz (2001) that mutations affecting the initial digit patterning are associated with strong negative pleiotropic effects and thus unlikely to be fixed in evolution. An important avenue of future research will be to directly test whether reevolved digits develop from conserved digit condensations retained after digit loss.     

EXPERIMENTAL EVOLUTION OF ACCELERATED DEVELOPMENT IN DROSOPHILA. 1. DEVELOPMENTAL SPEED AND LARVAL SURVIVAL

Developmental time is a trait of great relevance to fitness in all organisms. In holometabolous species that occupy ephemeral habitat, like Drosophila melanogaster, the impact of developmental time upon fitness is further exaggerated. We explored the trade-offs surrounding developmental time by selecting 10 independent populations from two distantly related selection treatments (CB_1-5 and CO_1-5) for faster development. After 125 generations, the resulting accelerated populations (ACB_1-5 and ACO_1-5) displayed net selection responses for development time of -33.4 hours (or 15%) for ACB and -38.6 hours (or 17%) for ACO. Since most of the change in egg-to-adult developmental time was accounted for by changes in larval duration, the “accelerated” larvae were estimated to develop 25-30% faster than their control/ancestor populations. The responses of ACB and ACO lines were remarkably parallel, despite being founded from populations evolved independently for more than 300 generations. On average, these “A” populations developed from egg to adult in less than eight days and produced fertile eggs less than 24 hours after emerging. Accelerated populations showed no change in larval feeding rate, but a reduction in pupation height, the latter being a trait relating to larval energetic expenditure in wandering prior to pupation. This experiment demonstrates the existence of a negative evolutionary correlation between preadult developmental time and viability, as accelerated populations experienced a severe cost in preadult survivorship. In the final assay generation, viability of accelerated treatments had declined by more than 10%, on average. A diallel cross demonstrated that the loss of viability in the ACO lines was not due to inbreeding depression. These results suggest the existence of a rapid development syndrome, in which the fitness benefits of fast development are balanced by fitness costs resulting from reduced preadult survivorship, marginal larval storage of metabolites, and reduced adult size.     

木姜子属及山胡椒属的平行演化

本文阐述樟科木姜子属及山胡椒属两者在形态、分布、起源及演化等方面有许多共同之处,不仅在属内具有平行演化的情况,而且各自平行演化成单花木姜子属Dodecade-nia和单花山胡椒属Iteadaphne。同时两者又分别自4药室的拟檫木属Parasassafras和2药室的黄脉檫木属Sinosassafras演化而来。本文将单花木姜子亚属Litsea subg.UniflosYang et P.H.Huang归入单花木姜子属,并把Litsea monantha Yang et P.H.Hu-ang一种作为单花木姜子(原变种)Dodecadenia grandiflora Nees var.grandiflora的新异名,恢复了单花山胡椒属Iteadaphne B1.,并将香面叶Lindera caudata(Nees)Hook.f.重新组合归入该属为I.caudata(Nees)H.W.Li,comb.nov。此外,本文还发表了一个新属即黄脉檫木属Sinosassafras H.W.Li,gen.nov.,它具有2药室花药而不同于其平行演化的拟檫木属。     

THE EVOLUTION OF DIAPAUSE IN THE KILLIFISH FAMILY RIVULIDAE (ATHERINOMORPHA,CYPRINODONTIFORMES): A MOLECULAR PHYLOGENETIC AND BIOGEOGRAPHIC PERSPECTIVE

Phylogenetic relationships within the family Rivulidae (order Cyprinodontiformes) are investigated using 1972 aligned base pairs of mitochondrial DNA (mtDNA) for samples representing 66 species. Genes analyzed include those encoding the 12S ribosomal RNA; transfer RNAs for valine, glutamine, methionine, tryptophan, alanine, asparagine, cysteine, and tyrosine; complete NADH dehydrogenase subunit II; and part of cytochrome oxidase I. Parsimony analysis of the aligned mtDNA sequences results in a single most parsimonious tree. The phylogeny reveals two independent origins of developmental diapause within the family Rivulidae. It is unlikely that diapause evolved de novo in each group, suggesting that the presence or absence of diapause is the result of developmental switches between alternative stabilized pathways. Phylogeny of the family Rivulidae shows high concordance with predictions derived from the geological history of South America and Central America. Basal lineages in the rivulid phylogeny are distributed primarily on geologically old areas, whereas more nested lineages occur in geologically younger areas. However, there is little concordance between the molecular phylogeny and currently available morphological hypotheses and existing taxonomies. Based on the mtDNA phylogeny, the genera Pterolebias, Rivulus, Pituna, and Plesiolebias are considered nonmonophyletic and warrant taxonomic reassessment.     

LABORATORY EVOLUTION OF LIFE-HISTORY TRAITS IN THE BEAN WEEVIL (ACANTHOSCELIDES OBTECTUS): THE EFFECTS OF SELECTION ON DEVELOPMENTAL TIME IN POPULATIONS WITH DIFFERENT PREVIOUS HISTORY

In this study we examined the direct and correlated responses for fast and slow preadult development time in three laboratory populations of the bean weevil (Acanthoscelides obtectus). The first population (“base,” B) has experienced laboratory conditions for more than 10 years; the second (“young,” Y) and the third (“old,” O) populations were selected for early and late reproduction, respectively, before the onset of the present experiments. All three populations are successfully selected for both fast and slow preadult development. The realized heritabilities are very similar in all populations, suggesting a similar level of the additive genetic variance for preadult development. We studied the correlated responses on the following life-history traits: egg-to-adult viability, wet body weight, early fecundity, late fecundity, total realized female fecundity, and adult longevity. All life-history traits examined here, except for the egg-to-adult viability, are affected by selection for preadult development in at least in one of the studied populations. In all three populations, beetles selected for slow preadult development are heavier and live longer than those from the fast-selected lines. The findings with respect to adult longevity are unexpected, because the control Y and O populations, selected for short- and long-lived beetles, respectively, do not show significant differences in preadult development. Thus, our results indicate that some kind of asymmetrical correlated responses occur for preadult development and adult longevity each time that direct selection has been imposed on one or the other of these two traits. In contrast to studies with Drosophila, it appears that for insect species that are aphagous as adults, selection for preadult development entails selection for alleles that also change the adult longevity, but that age-specific selection (applied in the Y and O populations) mostly affects the alleles that have no significant influence on the preadult development. Implications of these findings on the developmental and evolutionary theories of aging are also discussed.