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Fluctuating asymmetry in bracts and leaves: mean-scaled fluctuating asymmetries (±standard error) for lobe length. From left to right: the basal leaf, the proximate leaf, the distal leaf, the lower bract, and the upper bract. The values are corrected for measurement error (r 2 m-side) as described in Pélabon et al. (2004)
Source publication
The Berg hypothesis posits that, in plants with specialized pollination systems, floral characters should evolve to become
integrated with each other and decoupled from vegetative characters. We test this hypothesis by comparing serially homologous
and morphologically similar characters in leaves and involucral bracts in the Neotropical vine Dalech...
Contexts in source publication
Context 1
... mean-scaled fluctuating asymmetries of bracts and leaves were very similar (Fig. 5), and the fraction of phe- notypic variation that can be ascribed to developmental variation was in fact higher in bract lengths than in either leaf lengths or widths (Table 6). This suggests that the two organ systems are about equally developmentally stable, but that the developmental sources of variation become relatively more ...
Context 2
... and Var[sig. FA] is the variance of signed FA, %Dev is the % of phenotypic variance due to developmental variation, and N is the sample size Hansen et al. 2006), and has also been corrected for measurement error by subtracting r 2 m -side given in Table 1 from both the nominator and the denominator. Measurement-corrected FA is given in Fig. 5 correlations at the within-and among-individual levels (Armbruster 1991). Furthermore, the lack of genetic vari- ation in leaves predicts that they should be evolutionary ...
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Citations
... Wagner and Altenberg 1996), and metazoan diversification (Gerhart and Kirschner 2007) to specific evolutionary pathways. Evolvability is an explanatory tool for a variety of evolutionary trajectories in specific traits, including body shape (Bergmann et al. 2020), the stability of wing shape compared to the lability of life history traits in Drosophila (Houle et al. 2017), or differences between vegetative and floral traits (Hansen et al. 2007). ...
Essays on evolvability from the perspectives of quantitative and population genetics, evolutionary developmental biology, systems biology, macroevolution, and the philosophy of science.
Evolvability—the capability of organisms to evolve—wasn't recognized as a fundamental concept in evolutionary theory until 1990. Though there is still some debate as to whether it represents a truly new concept, the essays in this volume emphasize its value in enabling new research programs and facilitating communication among the major disciplines in evolutionary biology. The contributors, many of whom were instrumental in the development of the concept of evolvability, synthesize what we have learned about it over the past thirty years. They focus on the historical and philosophical contexts that influenced the emergence of the concept and suggest ways to develop a common language and theory to drive further evolvability research.
The essays, drawn from a workshop on evolvability hosted in 2019–2020 by the Center of Advanced Study at the Norwegian Academy of Science and Letters, in Oslo, provide scientific and historical background on evolvability. The contributors represent different disciplines of evolutionary biology, including quantitative and population genetics, evolutionary developmental biology, systems biology, and macroevolution, as well as the philosophy of science. This plurality of approaches allows researchers in disciplines as diverse as developmental biology, molecular biology, and systems biology to communicate with those working in mainstream evolutionary biology. The contributors also discuss key questions at the forefront of research on evolvability.
Contributors:J. David Aponte, W. Scott Armbruster, Geir H. Bolstad, Salomé Bourg, Ingo Brigandt, Anne Calof, James M. Cheverud, Josselin Clo, Frietson Galis, Mark Grabowski, Rebecca Green, Benedikt Hallgrímsson, Thomas F. Hansen, Agnes Holstad, David Houle, David Jablonski, Arthur Lander, Arnaud LeRouzic, Alan C. Love, Ralph Marcucio, Michael B. Morrissey, Laura Nuño de la Rosa, Øystein H. Opedal, Mihaela Pavličev, Christophe Pélabon, Jane M. Reid, Heather Richbourg, Jacqueline L. Sztepanacz, Masahito Tsuboi, Cristina Villegas, Marta Vidal-García, Kjetil L. Voje, Andreas Wagner, Günter P. Wagner, Nathan M. Young
... This nonge ne tic variation can be ecologically impor tant, yielding direct insights into form-function relationships, as well as patterns of stabilizing and canalizing se lection. Iterative plant organs also promote direct investigation into the evolutionary significance of phenotypic and ge ne tic integration and modularity (e.g., Berg 1960;Hansen et al. 2007;Pélabon et al. 2011; see reviews in Armbruster et al. 2014;Conner and Lande 2014). Fi nally, most plants are easy to clone, allowing investigators to address directly environmental sources of phenotypic (co)variation (but see the cautionary notes in Schwaegerle et al. 2000;Schwaegerle 2005). ...
... Flowers are modular units whose variation is often quasi-independent of variation in vegetative structures (Berg 1960, Armbruster et al. 1999, 2014Hansen et al. 2007;Pélabon et al. 2011;Conner and Lande 2014;). This floral-vegetative modularity should enhance evolvability of both sets of traits in the face of conflicting se lection on floral and vegetative traits. ...
Essays on evolvability from the perspectives of quantitative and population genetics, evolutionary developmental biology, systems biology, macroevolution, and the philosophy of science.
Evolvability—the capability of organisms to evolve—wasn't recognized as a fundamental concept in evolutionary theory until 1990. Though there is still some debate as to whether it represents a truly new concept, the essays in this volume emphasize its value in enabling new research programs and facilitating communication among the major disciplines in evolutionary biology. The contributors, many of whom were instrumental in the development of the concept of evolvability, synthesize what we have learned about it over the past thirty years. They focus on the historical and philosophical contexts that influenced the emergence of the concept and suggest ways to develop a common language and theory to drive further evolvability research.
The essays, drawn from a workshop on evolvability hosted in 2019–2020 by the Center of Advanced Study at the Norwegian Academy of Science and Letters, in Oslo, provide scientific and historical background on evolvability. The contributors represent different disciplines of evolutionary biology, including quantitative and population genetics, evolutionary developmental biology, systems biology, and macroevolution, as well as the philosophy of science. This plurality of approaches allows researchers in disciplines as diverse as developmental biology, molecular biology, and systems biology to communicate with those working in mainstream evolutionary biology. The contributors also discuss key questions at the forefront of research on evolvability.
Contributors:J. David Aponte, W. Scott Armbruster, Geir H. Bolstad, Salomé Bourg, Ingo Brigandt, Anne Calof, James M. Cheverud, Josselin Clo, Frietson Galis, Mark Grabowski, Rebecca Green, Benedikt Hallgrímsson, Thomas F. Hansen, Agnes Holstad, David Houle, David Jablonski, Arthur Lander, Arnaud LeRouzic, Alan C. Love, Ralph Marcucio, Michael B. Morrissey, Laura Nuño de la Rosa, Øystein H. Opedal, Mihaela Pavličev, Christophe Pélabon, Jane M. Reid, Heather Richbourg, Jacqueline L. Sztepanacz, Masahito Tsuboi, Cristina Villegas, Marta Vidal-García, Kjetil L. Voje, Andreas Wagner, Günter P. Wagner, Nathan M. Young
... In a canonical study of correlation patterns in plants, Berg (1960) showed that plants visited by specialized pollinators had lower correlations between floral and vegetative traits, but these traits remained correlated in plants pollinated by the wind or unspecialized insects. This pattern has also been reported with respect to the involucral bracts of Dalechampia scandens, which has a specialized pollination system based on resin-collecting bees (Hansen et al. 2007). ...
There is a widespread view that the process of adaptation in complex systems is made difficult due to an evolutionary cost of complexity that is reflected in lower evolvability. This line of reasoning suggests that organisms must have special properties to overcome this cost, such as integration, modularity, and robustness, and that the reduction in the rate of evolution and variational constraints could help explain why organisms might not respond to selection. Here, we discuss the issues that arise from this conviction and highlight an alternative view where complexity represents an opportunity by increasing the evolutionary potential of a population. We highlight the lack of evidence supporting the influence of complexity on evolvability. Empirical data on the patterns of contemporary selection are critical for understanding this relationship.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 53 is November 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... Both have long been recognised as potentially significant to evolvability (Wagner and Altenberg, 1996;Mitteroecker, 2009;Berg, 1960;Hansen et al., 2007;Lipson et al., 2002;Lipson, 2007;Melo et al., 2016;Conrad, 2017;Hansen, 2003;Yu and Gerstein, 2006;Hallinan, 2004). Both can facilitate reusability and separation of concerns in systems designed by humans: properties which can permit robustness in natural systems (Lipson, 2007). ...
This thesis is concerned with the evolution of hierarchical modules in a model of gene regulation, and the consequences thereof for evolvability. Developmental processes map genotypes to phenotypes, and translate random variation at the genetic level into biased, selectable variation at the phenotypic level. These developmental processes are themselves subject to evolution by natural selection and it might be the case that natural selection favours developmental architectures that facilitate phenotypic variation that is adaptive and enhances evolvability. One manner of developmental organisation that has inspired much interest is modular hierarchy. Such hierarchy - where one gene directs many others - has the potential to be very important to evolvability because it effectively rescales the variability of phenotypes, enabling natural selection to search combinations of modules rather than combinations of individual genes. However, the conditions where natural selection favours hierarchical organisation and the conditions where its consequences enable such rescaling are not well understood. Considering a developmental model based on a recurrent regulatory process, we describe conditions where natural selection favours the evolution of single-layer hierarchical modular structures, where independent ‘switch’ genes direct independent subsets of genes. We show that these structures increase evolvability by rescaling the genetic neighbourhood of phenotypes, from combinations of genes to combinations of modules, and that this makes high-fitness phenotypes more accessible to natural selection. This improved evolvability enables a micro-evolutionary process to better exploit a changing or static modular environment so long as sufficient long-term variation is maintained. We then investigate the underlying cause of the evolution of hierarchy. Interestingly, we find that the observable increase in evolvability (in particular, the ability to rescale the variability of phenotypes) is not required for natural selection to favour hierarchy in this model. Rather, hierarchy evolves due to a selective pressure for efficient phenotypic expression and because it is an efficient organisation for increasing the expression of many genes given limited regulatory connections. Thereby, we show that - in some cases - the causes and consequences of developmental hierarchy are not the same. That is, hierarchy evolves - and it increases evolvabilty - but increased evolvability need not be the reason it was favoured by selection.
... Distinguishing levels is important because the causes (and consequences) of integration/modularity differ by level. That traditional hierarchy, however, oversimplifies current conceptions of modularity in that modularity is now recognized at another level, the one most crucial to current theories of modularity: the genotype-phenotype map (Hallgrimsson et al., 2009;Hansen et al., 2007;Wagner & Altenberg, 1996), which bridges the levels of individual and populations. ...
... Berg (1960) and Olson and Miller (1958) analyzed correlation matrices. Berg's analysis of the ecological significance of correlation pleiades continues to stimulate research (e.g., Armbruster et al., 1999;Conner & Sterling, 1996;Hansen et al., 2007). Most of the metrics and methods can be extended to analyses of evolutionary correlations. ...
... We do often need a summary statistic when comparing degrees of modularity across datasets. In particular, we do often want to know whether some species are more or less modular than others (Bell et al., 2011;Machado et al., 2018;Marroig et al., 2009) and we may also want to know whether one ontogenetic stage is more modular than others (Ackermann, 2005;Goswami et al., 2012;Ivanovic et al., 2005;Zelditch & Carmichael, 1989) or whether some structures are more modular than others in particular lineages (Haber, 2015;Hansen et al., 2007;Young & Hallgrímsson, 2005). The question is whether a simple summary obscures valuable information. ...
Modularity is now generally recognized as a fundamental feature of organisms, one that may have profound consequences for evolution. Modularity has recently become a major focus of research in organismal biology across multiple disciplines including genetics, developmental biology, functional morphology, population and evolutionary biology. While the wealth of new data, and also new theory, has provided exciting and novel insights, the concept of modularity has become increasingly ambiguous. That ambiguity is underlain by diverse intuitions about what modularity means, and the ambiguity is not merely about the meaning of the word—the metrics of modularity are measuring different properties and the methods for delimiting modules delimit them by different, sometimes conflicting criteria. The many definitions, metrics and methods can lead to substantial confusion not just about what modularity means as a word but also about what it means for evolution. Here we review various concepts, using graphical depictions of modules. We then review some of the metrics and methods for analyzing modularity at different levels. To place these in theoretical context, we briefly review theories about the origins and evolutionary consequences of modularity. Finally, we show how mismatches between concepts, metrics and methods can produce theoretical confusion, and how potentially illogical interpretations can be made sensible by a better match between definitions, metrics, and methods.
Highlights
Modularity is a fundamental features of organisms, with potentially profound consequences for evolution. However, with expansion to new systems and scales of study, the concept of modularity has become increasing ambiguous. Here we map intuitions, metrics, and methods regarding modularity, discuss how their mismatch can create incoherence, and demonstrate how to untangle the confusion surrounding this core concept in organismal and evolutionary biology.
... In Clerodendrum, the style and stamen move in a direction opposite to each other, and they do so in a coordinated manner. In general, correlations among floral traits are higher than correlations among vegetative traits in plants because flowers are under direct selection (Berg 1959, Hansen et al. 2007). As expected, the correlation between the positions of style and stamens at different time points in a floral lifetime is high (Fig. 3). ...
Over 70% of flowering plants are hermaphroditic, with male and female parts in the same flower. Hermaphroditism is cost-effective because a common investment in reward and attractive structures yields benefits through both male and female reproductive success. However, the advantage is accompanied by an increased risk of self-pollen deposition, which is disadvantageous for both self-compatible and self-incompatible species. Hermaphroditic plants reduce self-pollen deposition by separating sporophylls (male and female reproductive parts) either spatially (herkogamy) or temporally (dichogamy). In movement-assisted dichogamy, both sporophylls are involved in a coordinated motion, where they move in opposite directions. However, the effectiveness of this adaptation in reducing self-pollen deposition may be compromised at the point when the sporophylls cross each other and are close enough to interfere, resulting in a transition phase problem. The solution to this problem lies in the details of the spatiotemporal dynamics of the sporophylls in relation to their reproductive maturity. We studied these details across the floral lifetime of a protandrous shrub Clerodendrum infortunatum (Lamiaceae), in rainforest fragments of the Western Ghats, India. We took photos of flowers at regular time intervals and measured sporophyll angles from the images. We also carried out a field experiment to determine stigma receptivity. The findings suggest that the effectiveness of dichogamy is maximised through two properties of the transition phase: physical resistance to self-pollen deposition by narrow stigma lobe opening, and chemical non-receptivity of the stigma during this phase. This study emphasises the importance of accessory adaptations in movement-assisted dichogamy to tackle the transition phase problem, which is inherent in this particular form of dichogamy.
... One of the earliest and most cogent hypotheses about patterns of trait variation and covariation in flowers was put forward by Raissa Berg [1960; but see also Stebbins (1951) and Sporne (1954) for earlier, contrasting approaches]. She and subsequent researchers have emphasized the role of natural selection in generating these patterns (see reviews and discussions in Conner and Sterling, 1996;Armbruster et al., 1999Armbruster et al., , 2004Armbruster et al., , 2014Hansen et al., 2007;Pélabon et al., 2011Pélabon et al., , 2013Murren 2012;Conner and Lande, 2014;Wanderley et al., 2016), but other factors, such as genetic and developmental constraints, can also be involved (Gould and Lewontin, 1979;Gould, 2002). The 'Berg hypothesis' in its original form can be summarized as the expectation that the variation in traits of specialized flowers will be largely uncorrelated with variation in vegetative and other non-floral traits (Berg, 1960;Conner and Lande, 2014). ...
Background and aims:
The Berg hypothesis proposes that specialized-flower traits experience stronger stabilizing selection than non-floral structures and predicts that variation in specialized-flower traits will be mostly uncorrelated with variation in non-floral traits. Similarly, adaptive-accuracy theory predicts lower variation (as a proportion of the mean) in floral traits than in non-floral ones. Both hypotheses can be extended to comparisons between floral traits, where different parts of the flower can be expected to experience different strengths of stabilizing selection, resulting in contrasting patterns of variation. The present study tests these ideas by analysing variation/covariation in those floral traits influencing the location of pollen placement on, and stigma contact with, pollinators ('pollination-mechanics traits', PMTs) in relation to variation/covariation in non-floral traits and floral traits not directly involved in the mechanics of pollination. The prediction was that PMTs are canalized (buffered against genetic and environmental variation) relative to attraction traits, as manifested in lower variances and modular independence.
Methods:
Floral and inflorescence structures of ten species of triggerplants (Stylidium, Stylidiaceae) in south-western Australia were measured; the data were analysed using multivariate and bivariate approaches to detect modular structure of floral and non-floral traits and assess evidence for canalization of PMTs.
Key results:
Only six of the ten species had PMTs with smaller correlation coefficients than attraction traits, in contrast to the Berg expectation. However, allometric and variance patterns were generally consistent with the predictions of an extended Berg hypothesis and adaptive accuracy. There was modular separation of most floral traits from non-floral traits and clear intra-floral modular structure. PMTs showed lower proportional variation and shallower allometric slopes than pollinator-attraction traits in nine and eight, respectively, of ten species.
Conclusions:
This study demonstrates the value of allometric and variance analyses (in addition to correlation) in assessing the evolutionary significance of floral-trait stability and plasticity.
... Because effective pollen transfer depends on precise fit of flowers and pollinators, floral traits in animalpollinated species are expected to be less sensitive to environmental variation and therefore less variable than vegetative traits (Berg, 1960;Armbruster et al., 1999;P elabon et al., 2011). However, it is not well understood whether and how the different environmental sensitivities of floral and vegetative traits affect their evolvabilities, and the relationship between genetic and environmental (nongenetic) variances (Conner & Via, 1993;Hansen et al., 2007). An interesting possibility is that pollinatormediated stabilizing selection on floral dimensions could lead both to environmental canalization and to loss of standing genetic variation, therefore resulting in reduced evolvability of traits that are important for adaptation to novel pollinator communities. ...
In the event of a community turnover, population decline, or complete disappearance of pollinators, animal‐pollinated plants may respond by adapting to novel pollinators or by changing their mating system. The ability of populations to adapt is determined by their ability to respond to novel selection pressures, i.e. their evolvability. In the short term, evolvability is determined by standing genetic variation in the trait under selection.
To evaluate the evolutionary potential of plant reproductive systems, I compiled genetic‐variance estimates for a large selection of floral traits mediating shifts in pollination and mating systems. Then, I computed evolvabilities and compared these among trait groups and against the evolvabilities of vegetative traits.
Evolvabilities of most floral traits were substantial yet tended to be lower than the median for vegetative traits. Among floral traits, herkogamy (anther–stigma distance), floral‐display traits and perhaps floral‐volatile concentrations had greater‐than‐average evolvabilities, while the evolvabilities of pollinator‐fit traits were below average.
These results suggest that most floral traits have the potential to evolve rapidly in response to novel selection pressures, providing resilience of plant reproductive systems in the event of changing pollinator communities.
... This difference between floral and foliar integration coincides with the original hypothesis predicted by Berg (1960), in which she stated that trait correlations should be less canalised and more plastic in vegetative than in floral modules, as the latter are subject to strong pollinator-mediated selection. Although other works have reported independence in the patterns of correlation among reproductive and vegetative plant parts (Conner & Sterling, 1996;Hansen, Pélabon, & Armbruster, 2007;Pélabon, Armbruster, & Hansen, 2011), they usually include traits from different vegetative modules (e.g. stems and leaves) involving only morphological, rather than functional vegetative traits. ...
Changes in resource availability, functional demands, hormonal regulation and developmental constraints can promote differences in the expression of leaf traits during plant development and foster changes in the targets of natural selection. As a consequence, the pattern and magnitude of covariation among traits, and therefore their phenotypic integration and modularity are equally expected to change throughout ontogeny. However, these changes have not been described yet.
We measured leaf economic, defensive and morphological traits in plants of Turnera velutina and estimated the magnitude and pattern of foliar integration and modularity for juvenile and reproductive individuals. In addition, we assessed the relationship between plant biomass and foliar integration within and among ontogenetic stages.
Both the pattern and magnitude of foliar integration changed across plant ontogeny. Foliar integration was lower in juvenile than in reproductive plants, and the pattern of phenotypic integration and modularity was different between ontogenetic stages, whereas leaves from juvenile plants showed two functional modules related to plant defence and leaf economy, traits from reproductive plants had greater interconnectivity and hence lower modularity.
The relationship between plant biomass and foliar integration was negative within each ontogenetic stage but positive between ontogenetic stages, suggesting that processes intrinsic to plant development influenced the magnitude of foliar integration to a greater extent than plant size.
Our findings indicate that plants can change the patterns of covariation among leaf traits during their development. However, a lower foliar integration in juvenile plants could allow for greater lability to explore a multi‐trait phenotypic space, canalisation of leaf attributes along ontogeny should promote greater phenotypic integration, constraining the number of multi‐trait combinations that plants can express. Hence, we suggest that ontogenetic changes in foliar integration allow plants to deal with changing selective dynamics and physiological priorities along their development.
A plain language summary is available for this article.
... Much of the spectacular trait and species diversity of flowering plants can be attributed to the evolution of flowers and interactions between plants and pollinators (Kay et al., 2006;Kay and Sargent, 2009;van der Niet and Johnson, 2012;Armbruster, 2014). Floral trait variation is often conserved at the species level, and is more canalized than variation in vegetative traits in response to environmental fluctuations (Berg, 1960;Armbruster et al., 1999;Hansen et al., 2007;Pélabon et al., 2011Pélabon et al., , 2013. Such canalization and reduced variation in floral traits implies that the plant-pollinator interaction often imposes strong selection for certain floral phenotypes (Cresswell, 1998;Rosas-Guerrero et al., 2011;Pélabon et al., 2013). ...
Background and aims:
Many plant-pollinator interactions are mediated by floral scents that can vary among species, among populations within species and even among individuals within populations. This variation could be innate and unaffected by the environment, but, because many floral volatiles have amino-acid precursors, scent variation also could be affected by differences in nutrient availability among environments. In plants that have coevolved with specific pollinators, natural selection is likely to favour low phenotypic plasticity in floral scent even under different conditions of nutrient availability if particular scents or scent combinations are important for attracting local pollinators.
Methods:
Clonal pairs of multiple seed-families of two Lithophragma bolanderi (Saxifragaceae) populations were subjected to a high and a low nutrient treatment. These plants are pollinated primarily by host-specific Greya moths. It was evaluated how nutrient treatment affected variation in floral scent relative to other vegetative and reproductive traits.
Key results:
Floral scent strength (the per-flower emission rate) and composition were unaffected by nutrient treatment, but low-nutrient plants produced fewer and lighter leaves, fewer scapes and fewer flowers than high-nutrient plants. The results held in both populations, which differed greatly in the number and composition of floral scents produced.
Conclusions:
The results reveal a strong genetic component both to scent composition and emission level, and partly contrasts with the only previous study that has assessed the susceptibility of floral volatile signals to variation in the abundance of nutrients. These results, and the tight coevolutionary relationship between Lithophragma plants and their specialized Greya moth pollinators, indicate that reproductive traits important to coevolving interactions, such as the floral scent of L. bolanderi , may be locally specialized and more canalized than other traits important for plant fitness.
