Trends in flower symmetry evolution revealed through phylogenetic and developmental genetic advances

A striking aspect of flowering plant (angiosperm) diversity is variation in flower symmetry. From an ancestral form of radial symmetry (polysymmetry, actinomorphy), multiple evolutionary transitions have contributed to instances of non-radial forms, including bilateral symmetry (monosymmetry, zygomorphy) and asymmetry. Advances in flowering plant molecular phylogenetic research and studies of character evolution as well as detailed flower developmental genetic studies in a few model species (e.g. Antirrhinum majus, snapdragon) have provided a foundation for deep insights into flower symmetry evolution. From phylogenetic studies, we have a better understanding of where during flowering plant diversification transitions from radial to bilateral flower symmetry (and back to radial symmetry) have occurred. From developmental studies, we know that a genetic programme largely dependent on the functional action of the CYCLOIDEA gene is necessary for differentiation along the snapdragon dorsoventral flower axis. Bringing these two lines of inquiry together has provided surprising insights into both the parallel recruitment of a CYC-dependent developmental programme during independent transitions to bilateral flower symmetry, and the modifications to this programme in transitions back to radial flower symmetry, during flowering plant evolution.     

Did internal transport,rather than directed locomotion,favor the evolution of bilateral symmetry in animals?

The standard explanation for the origin of bilateral symmetry is that it conferred an advantage over radial symmetry for directed locomotion. However, recent developmental and phylogenetic studies suggest that bilateral symmetry may have evolved in a sessile benthic animal, predating the origin of directed locomotion. An evolutionarily feasible alternative explanation is that bilateral symmetry evolved to improve the efficiency of internal circulation by affecting the compartmentalization of the gut and the location of major ciliary tracts. This functional design principle is illustrated best by the phylum Cnidaria where symmetry varies from radial to tetraradial, biradial and bilateral. In the Cnidaria, bilateral symmetry is manifest most strongly in the internal anatomy and the disposition of ciliary tracts. Furthermore, the bilaterally symmetrical Cnidaria are typically sessile and, in those bilaterally symmetrical cnidarians that undergo directed locomotion, the secondary body axis does not bear a consistent orientation to the direction of locomotion as it typically does in Bilateria. Within the Cnidaria, the hypothesized advantage of bilateral symmetry for internal circulation can be tested by experimental analysis and computer modeling of fluid mechanics. The developmental evolution of symmetry within the Cnidaria can be further explored through comparative gene expression studies among species whose symmetry varies.     

Are human preferences for facial symmetry focused on signals of developmental instability?

Humans find symmetrical faces more attractive than are asymmetricalfaces. Evolutionary psychologists claim that our preferencefor symmetry can be explained in the context of mate choicebecause symmetry is an honest indicator of the genetic qualityof potential mates. These arguments assume that asymmetry inhuman faces is fluctuating asymmetry (FA), because this formof asymmetry can be revealing of developmental instability.However, no study has yet examined the characteristics of facialasymmetry. Here we provide the first detailed study of the patternsof asymmetry in human faces. We measured asymmetry in 35 facialtraits. Although some traits had distributions characteristicof FA, many had distributions that characterize directionalasymmetry (DA); on average, both men and women had right hemi-facedominance. For DA traits we used deviations from the mean asymmetryas a measure of developmental instability. Our measures of asymmetryaccounted for a moderate proportion of the variance in perceivedsymmetry. Importantly, only FAs and random deviations from DAcontributed to people's perception of symmetry. DA was not importantin symmetry judgments. Faces rated as symmetrical were alsorated as attractive. Random deviations from DA were weakly relatedto women's attractiveness judgments of men's faces. DAs didnot influence attractiveness judgments. Our data suggest thatpeople focus on aspects of facial asymmetry that may be revealingof developmental instability. Further studies that isolate FAfrom other forms of asymmetry are required to accurately assessthe influence of developmental instability on the quality ofindividuals and its potential role in mate preferences.     

FLUCTUATING ASYMMETRY IN A SALIX HYBRID SYSTEM: THE IMPORTANCE OF GENETIC VERSUS ENVIRONMENTAL CAUSES

To examine the effects of hybridization and environmental stress on developmental instability, we examined fluctuating asymmetry (FA), the variance in random deviations from perfect symmetry in bilaterally symmetrical traits, for leaf symmetry in a Salix hybrid system. An abiotic environmental stress (water stress), an interspecific biotic stress (pathogen attack), and an intraspecific biotic stress (competition) were examined to determine which factors increase developmental instability. None of these three environmental stressors significantly increased FA. However, genetic stress through hybridization was detected; hybrid plants showed significantly higher levels of FA than parental species. In contrast to hybridization providing greater developmental stability through heterozygosity, these results suggest that complex, nonadditive interactions provided developmental stability and that developmental instability increased when coadapted gene complexes were disrupted through hybridization. In addition, plant biomass was significantly, negatively correlated with FA, suggesting that those individuals that were more able to buffer themselves against the disruptive effects of environmental stress may have a selective advantage over those that are less able to buffer themselves against these disruptive effects.     

Symmetry of the face in old age reflects childhood social status

The association of socioeconomic status (SES) with a range of lifecourse outcomes is robust, but the causes of these associations are not well understood. Research on the developmental origins of health and disease has led to the hypothesis that early developmental disturbance might permanently affect the lifecourse, accounting for some of the burden of chronic diseases such as coronary heart disease. Here we assessed developmental disturbance using bodily and facial symmetry and examined its association with socioeconomic status (SES) in childhood, and attained status at midlife. Symmetry was measured at ages 83 (facial symmetry) and 87 (bodily symmetry) in a sample of 292 individuals from the Lothian Birth Cohort 1921 (LBC1921). Structural equation models indicated that poorer SES during early development was significantly associated with lower facial symmetry (standardized path coefficient ?.25, p = .03). By contrast, midlife SES was not significantly associated with symmetry. The relationship was stronger in men (?.44, p = .03) than in women (?.12, p = .37), and the effect sizes were significantly different in magnitude (p = .004). These findings suggest that SES in early life (but not later in life) is associated with developmental disturbances. Facial symmetry appears to provide an effective record of early perturbations, whereas bodily symmetry seems relatively imperturbable. As bodily and facial symmetries were sensitive to different influences, they should not be treated as interchangeable. However, markers of childhood disturbance remain many decades later, suggesting that early development may account in part for associations between SES and health through the lifecourse. Future research should clarify which elements of the environment cause these perturbations.     

Color pattern analysis of nymphalid butterfly wings: revision of the nymphalid groundplan

To better understand the developmental mechanisms of color pattern variation in butterfly wings, it is important to construct an accurate representation of pattern elements, known as the "nymphalid groundplan". However, some aspects of the current groundplan remain elusive. Here, I examined wing-wide elemental patterns of various nymphalid butterflies and confirmed that wing-wide color patterns are composed of the border, central, and basal symmetry systems. The central and basal symmetry systems can express circular patterns resembling eyespots, indicating that these systems have developmental mechanisms similar to those of the border symmetry system. The wing root band commonly occurs as a distinct symmetry system independent from the basal symmetry system. In addition, the marginal and submarginal bands are likely generated as a single system, referred to as the "marginal band system". Background spaces between two symmetry systems are sometimes light in coloration and can produce white bands, contributing significantly to color pattern diversity. When an element is enlarged with a pale central area, a visually similar (yet developmentally distinct) white band is produced. Based on the symmetric relationships of elements, I propose that both the central and border symmetry systems are comprised of "core elements" (the discal spot and the border ocelli, respectively) and a pair of "paracore elements" (the distal and proximal bands and the parafocal elements, respectively). Both core and paracore elements can be doubled, or outlined. Developmentally, this system configuration is consistent with the induction model, but not with the concentration gradient model for positional information.     

Similar genetic mechanisms underlie the parallel evolution of floral phenotypes

The repeated origin of similar phenotypes is invaluable for studying the underlying genetics of adaptive traits; molecular evidence, however, is lacking for most examples of such similarity. The floral morphology of neotropical Malpighiaceae is distinctive and highly conserved, especially with regard to symmetry, and is thought to result from specialization on oil-bee pollinators. We recently demonstrated that CYCLOIDEA2-like genes (CYC2A and CYC2B) are associated with the development of the stereotypical floral zygomorphy that is critical to this plant-pollinator mutualism. Here, we build on this developmental framework to characterize floral symmetry in three clades of Malpighiaceae that have independently lost their oil bee association and experienced parallel shifts in their floral morphology, especially in regard to symmetry. We show that in each case these species exhibit a loss of CYC2B function, and a strikingly similar shift in the expression of CYC2A that is coincident with their shift in floral symmetry. These results indicate that similar floral phenotypes in this large angiosperm clade have evolved via parallel genetic changes from an otherwise highly conserved developmental program.     

Evolution of GCYC, a Gesneriaceae homolog of CYCLOIDEA, within Gesnerioideae (Gesneriaceae)

Through recent advances in molecular developmental biology it has become clear that similar morphological traits may sometimes arise from different genetic bases. The molecular developmental biology of floral symmetry has been examined recently in detail and several genes important in controlling floral symmetry in diverse Asteridae have been identified. One of the most important among these is the floral symmetry gene CYCLOIDEA (CYC). We compared GCYC (the Gesneriaceae homolog of CYC) sequences in Gesneriaceae genera with the typical bilaterally symmetric flowers and genera with radial or near radial symmetry. Parsimony, Bayesian and maximum likelihood analyses of GCYC sequences among members of Gesnerioideae are mostly congruent with previous phylogenetic hypotheses, but suggest two unexpected generic positions: Diastema as sister to Gesneria, and Bellonia within Gloxinieae. In order to evaluate whether these results might be artifactual we obtained new gene sequences from chloroplast and nuclear ribosomal regions. These data disagree with GCYC regarding the placement of Diastema, but agree with GCYC regarding Bellonia. We did not find any mutations in GCYC that could explain the shift in symmetry and there were no consistent differences in molecular evolution between taxa with bilaterally or radially symmetric flowers. Likewise taxa with radial floral symmetry are not sister to each other showing that the loss of bilateral symmetry has occurred multiple times in parallel. Further investigations of GCYC expression will be necessary to determine if any of these independent events involved changes in the regulation of GCYC.     

Symmetry, sexual dimorphism in facial proportions and male facial attractiveness

Facial symmetry has been proposed as a marker of developmental stability that may be important in human mate choice. Several studies have demonstrated positive relationships between facial symmetry and attractiveness. It was recently proposed that symmetry is not a primary cue to facial attractiveness, as symmetrical faces remain attractive even when presented as half faces (with no cues to symmetry). Facial sexual dimorphisms ('masculinity') have been suggested as a possible cue that may covary with symmetry in men following data on trait size/symmetry relationships in other species. Here, we use real and computer graphic male faces in order to demonstrate that (i) symmetric faces are more attractive, but not reliably more masculine than less symmetric faces and (ii) that symmetric faces possess characteristics that are attractive independent of symmetry, but that these characteristics remain at present undefined.     

Evolutionary Trends in the Flowers of Asteridae: Is Polyandry an Alternative to Zygomorphy?

Background and Aims

Floral symmetry presents two main states in angiosperms, actinomorphy (polysymmetry or radial symmetry) and zygomorphy (monosymmetry or bilateral symmetry). Transitions from actinomorphy to zygomorphy have occurred repeatedly among flowering plants, possibly in coadaptation with specialized pollinators. In this paper, the rules controlling the evolution of floral symmetry were investigated to determine in which architectural context zygomorphy can evolve.

Methods

Floral traits potentially associated with perianth symmetry shifts in Asteridae, one of the major clades of the core eudicots, were selected: namely the perianth merism, the presence and number of spurs, and the androecium organ number. The evolution of these characters was optimized on a composite tree. Correlations between symmetry and the other morphological traits were then examined using a phylogenetic comparative method.

Key Results

The analyses reveal that the evolution of floral symmetry in Asteridae is conditioned by both androecium organ number and perianth merism and that zygomorphy is a prerequisite to the emergence of spurs.

Conclusions

The statistically significant correlation between perianth zygomorphy and oligandry suggests that the evolution of floral symmetry could be canalized by developmental or spatial constraint. Interestingly, the evolution of polyandry in an actinomorphic context appears as an alternative evolutionary pathway to zygomorphy in Asteridae. These results may be interpreted either in terms of plant–pollinator adaptation or in terms of developmental or physical constraints. The results are discussed in relation to current knowledge about the molecular bases underlying floral symmetry.Key words: Floral symmetry, architectural constraints, Asteridae, comparative analysis, composite tree, correlated evolution, evolutionary scenario     

Diverse radial symmetry among the Cambrian Fortunian fossil embryos from northern Sichuan and southern Shaanxi provinces,South China

The Cambrian Fortunian fossil embryos exhibit embryonic development of ancient animals and hence have important bearings on evolutionary developmental biology. They have radial symmetry, and may be early representatives of cnidarians. Here we report new material of three-dimensionally phosphatized fossil embryos from the Fortunian Kuanchuanpu Formation and coeval strata in northern Sichuan and southern Shaanxi provinces, South China. The new material includes previously reported fossil embryos assignable to Pseudooides prima with biradial symmetry or pseudo-hexaradial symmetry, Quadrapyrgites quadratacris with tetraradial symmetry, and Olivooides multisulcatus with pentaradial symmetry. Additionally, we recovered two new types of fossil embryos, i.e., Embryo I with hexaradial symmetry and Embryo II with octaradial symmetry, and they are tentatively suggested to represent new cnidarians. In contrast to the diverse radial symmetry of the Fortunian cnidarians, modern cnidarians exhibit stable tetraradial symmetry in medusozoans, biradial symmetry in anthozoans, and bilateral symmetry in siphonophores (Hydrozoa). The current study supports the view that the tetraradial symmetry of modern medusozoans is a surviving remnant of their Fortunian relatives.     

The Developmental Instability—Sexual Selection Hypothesis: A General Evaluation and Case Study

Developmental instability results from small, random perturbations to developmental processes of individual traits. Phenotypic outcomes of developmental instability include fluctuating asymmetry (FA, subtle deviations from perfect bilateral symmetry) and phenodeviance (minor morphological abnormalities). A great deal of research over the past 18 years has focused on the role of developmental instability in sexual selection. A driving force behind this research has been the developmental instability-sexual selection hypothesis, which posits that symmetry and lack of phenodeviance in secondary sexual traits are assessed by mates and rivals because they provide a reliable cue of individual genetic quality. The present article tests this hypothesis by evaluating its five main predictions using published results: expressions of developmental instability in secondary sexual traits should be (1) negatively correlated with mating success; (2) directly assessed by mates and sexual rivals; (3) heritable; (4) condition-dependent; and (5) negatively correlated with ornament size. The first two predictions receive considerable, though not ubiquitous, support from a range of animal species. However, FA in secondary sexual traits is generally not significantly heritable, indicating that FA is unlikely to reveal genetic quality that can be transmitted to offspring. Similarly, there is little evidence to support the predictions that FA is condition dependent, and that it is negatively phenotypically or genetically correlated with sexual trait size. Based on an evaluation of the evidence overall, it is concluded that this hypothesis is unlikely to be viable; it appears unlikely that mate choice for symmetry evolves by “good genes” sexual selection. Hypotheses that do not require asymmetry and phenodeviance to reveal heritable genetic quality may explain observed links between FA/phenodeviance and mating success. Results of a case study of Drosophila bipectinata are summarized, which reinforce this general conclusion. It is suggested that nonadditive genetic variation arising from an interaction between trait-specific developmental genes and genetic background may drive sexual selection for reducing developmental instability in some cases. Levels of developmental instability variation in a population may need to surpass a critical threshold for sexual selection to operate, possibly explaining some of the pronounced heterogeneity in the effect of developmental instability on sexual selection reported in the literature.     

Developmental regulatory genes and echinoderm evolution

Modified interactions among developmental regulatory genes and changes in their expression domains are likely to be an important part of the developmental basis for evolutionary changes in morphology. Although developmental regulatory genes are now being studied in an increasing number of taxa, there has been little attempt to analyze the resulting data within an explicit phylogenetic context. Here we present comparative analyses of expression data from regulatory genes in the phylum Echinodermata, considering the implications for understanding both echinoderm evolution as well as the evolution of regulatory genes in general. Reconstructing the independent evolutionary histories of regulatory genes, their expression domains, their developmental roles, and the structures in which they are expressed reveals a number of distinct evolutionary patterns. A few of these patterns correspond to interpretations common in the literature, whereas others have received little prior mention. Together, the analyses indicate that the evolution of echinoderms involved: (1) the appearance of many apomorphic developmental roles and expression domains, some of which have plesiomorphic bilateral symmetry and others of which have apomorphic radial symmetry or left-right asymmetry; (2) the loss of some developmental roles and expression domains thought to be plesiomorphic for Bilateria; and (3) the retention of some developmental roles thought to be plesiomorphic for Bilateria, although with modification in expression domains. Some of the modifications within the Echinodermata concern adult structures; others, transient larval structures. Some changes apparently appeared early in echinoderm evolution (> 450 Ma), whereas others probably happened more recently (< 50 Ma). Cases of likely convergence in expression domains suggest caution when using developmental regulatory genes to make inferences about homology among morphological structures of distantly related taxa.     

Facial masculinity and fluctuating asymmetry

Recently, women have been found to prefer the scent of symmetrical men and relatively masculine male faces more during the fertile (late follicular and ovulatory) phases of their menstrual cycles than during their infertile (e.g., luteal) phases. These findings make most theoretical sense if men's symmetry is associated with the masculinity of their faces and, therefore, men's symmetry and facial masculinity tap a shared underlying quality. This study examined associations between masculine facial features and nonfacial body symmetry as well as facial symmetry in samples of 141 men and 154 women. As predicted, a component of facial features that discriminates the sexes and reflects masculinization of the face significantly covaried with symmetry in men. No significant correlation was observed for women. These findings suggest that men's facial masculinity partly advertises underlying developmental stability.     

Developmental instability in cabbage aphid (Brevicoryne brassicae) populations exposed to heavy metal accumulated host plants

Random deviations from the perfect symmetry of normally bilaterally symmetrical characters exist during individual development as a result of various environmental conditions. Fluctuating asymmetry (FA) is often used as a measurement of developmental instability, and within-environmental variation (CV_e) is also considered as an indicator of developmental deviations. These two parameters may indicate the quality of the environmental habitat of organisms. For herbivore insects, such as aphids, any change in their host plants conditions is important and directly affects their development. The presented investigation revealed that both Lead (Pb) and Copper (Cu) accumulation in different host plants resulted in a significant amount of deviations from bilateral symmetry in cabbage aphid (Brevicoryne brassicae). Cabbage aphid populations showed higher FA and CV_e on heavy metal accumulated cabbage and radish than on non-contaminated cabbage and radish plants. However, the pattern between developmental instability and fitness measurements was inconsistent. Thus, this study does not support the hypothesis that asymmetry is a valuable bioindicator of developmental instability.     

An assessment of the homeostasis of development in man by dermatoglyphic indices]

Dermatoglyphic traits were examined in 176 inhabitants (39 families) of a village in Arkhangelsk Province. The level of bilateral symmetry and the similarity of the traits were determined in parents, in parents-children pairs, and between children. It is suggested that differences in the level of bilateral symmetry between children and the extent of similarity between children and parents may be used as a criterion of stability or developmental homeostasis in man.     

Asymmetry and Mating Success in a Periodical Cicada, Magicicada septendecim (Hemiptera: Cicadidae)

Phenotypic symmetry results from both a genetic predisposition and the influence of the developmental environment. Although most studies of mate choice and phenotypic asymmetry are couched in terms of active choice for ‘good genes’, an alternative viewpoint is to consider incidental mating biases that arise from the functional effects of asymmetrical phenotypes. This paper (i) discusses the specific situations in which symmetry‐based mate choice may be likely, and (ii) presents research on female mate choice and symmetry in the periodical cicada, Magicicada septendecim (L.). Male mating aggregations and lack of mating gifts or parental care make this species an ideal target for studying female choice for superior mates, and thus for a relationship between male symmetry and male mating success.     

Facial symmetry and judgements of apparent health: Support for a “good genes” explanation of the attractiveness–symmetry relationship

The “good genes” explanation of attractiveness posits that mate preferences favour healthy individuals due to direct and indirect benefits associated with the selection of a healthy mate. Consequently, attractiveness judgements are likely to reflect judgements of apparent health. One physical characteristic that may inform health judgements is fluctuating asymmetry as it may act as a visual marker for genetic quality and developmental stability. Consistent with these suggestions, a number of studies have found relationships between facial symmetry and facial attractiveness. In Study 1, the interplay between facial symmetry, attractiveness, and judgements of apparent health was explored within a partial correlation design. Findings suggest that the attractiveness–symmetry relationship is mediated by a link between judgements of apparent health and facial symmetry. In Study 2, an opposite-sex bias in sensitivity to facial symmetry was observed when judging health. Thus, perceptual analysis of symmetry may be an adaptation facilitating discrimination between potential mates on the basis of apparent health. The findings of both studies are consistent with a “good genes” explanation of the attractiveness–symmetry relationship and problematic for the claim that symmetry is attractive as a by-product of the ease with which the visual recognition system processes symmetric stimuli.     

Developmental stability and pollination

A number of different insect species (ranging from Diptera, Lepidoptera and Coleoptera to Hymenoptera) have been shown to discriminate between small degrees of asymmetry when visiting flowers or flower-like models. Such preferences for symmetry may have an innate basis. Small degrees of bilateral or radial asymmetry of flowers are considered to represent a measure of developmental instability, since deviations from perfect symmetry reflect the inability to maintain developmental precision during ontogeny. Environmental factors causing increased asymmetry in leaves and flowers include radioactive radiation, ultraviolet radiation, excess artificial fertilizer, various pollutants, extreme saline conditions, herbivory and competition. Genetic factors that contribute to increased asymmetry in plants include homozygosity, hybridization, mutation and quantitative genetic differences among individuals. Insect preferences for symmetric flowers increase reproductive success of both pollen donors and recipients by affecting seed set and embryo abortion. The ability of insects to discriminate between flowers of superior and inferior quality is hypothesized to depend on the level of developmental instability of the perceptive apparatus of insects. Hence, asymmetry of insects may have consequences for plant reproductive success and mating patterns. Received: 18 November 1999 / Accepted: 15 December 1999     

Starlings can categorize symmetry differences in dot displays

Fluctuating asymmetry is an estimate of developmental stability and, in some cases, the asymmetry of morphological traits can reflect aspects of individual fitness. As asymmetry can be a marker for fitness, it has been proposed that organisms could use morphological asymmetry as a direct visual cue during inter- and intraspecific encounters. Despite some experimental evidence to support this prediction, the perceptual abilities of animals to detect and respond to symmetry differences have been largely overlooked. Studying the ability of animals to perceive symmetry and factors that affect this ability are crucial to assessing whether fluctuating asymmetry could be used as a visual cue in nature. In this study, we investigated the ability of wild-caught European starlings Sturnus vulgaris to learn to discriminate symmetry from asymmetry in random dot patterns through operant learning experiments. The birds did not possess a spontaneous preference for either symmetry or asymmetry. The birds learned a symmetry preference, although the learning process took longer than that previously reported for pigeons Columba livia and was more error prone. After being trained to discriminate symmetry differences in random dot patterns, birds successfully transferred their symmetry discrimination abilities to a set of novel stimuli that they had not previously seen. This indicates that starlings can form a mental categorization of visual stimuli on the basis of a somewhat generalized symmetry phenomenon. We discuss these findings in relation to the probability that birds use fluctuating asymmetry as a visual cue.