Turning induced plasticity into refined adaptations during range expansion.

Robustness against environmental fluctuations within an adaptive state should preclude exploration of new adaptive states when the environment changes. Here, we study transitions between adaptive associations of feather structure and carotenoid uptake to understand how robustness and evolvability can be reconciled. We show that feather modifications induced by unfamiliar carotenoids during a range expansion are repeatedly converted into precise coadaptations of feather development and carotenoid accommodation as populations persist in a region. We find that this conversion is underlain by a uniform and coordinated increase in the sensitivity of feather development to local carotenoid uptake, indicative of cooption and modification of the homeostatic mechanism that buffers feather growth in the evolution of new adaptations. Stress-buffering mechanisms are well placed to alternate between robustness and evolvability and we suggest that this is particularly evident in adaptations that require close integration between widely fluctuating external inputs and intricate internal structures.

Cycles of external dependency drive evolution of avian carotenoid networks.

All organisms depend on input of exogenous compounds that cannot be internally produced. Gain and loss of such dependencies structure ecological communities and drive species' evolution, yet the evolution of mechanisms that accommodate these variable dependencies remain elusive. Here, we show that historical cycles of gains and losses of external dependencies in avian carotenoid-producing networks are linked to their evolutionary diversification. This occurs because internalization of metabolic controls-produced when gains in redundancy of dietary inputs coincide with increased branching of their derived products-enables rapid and sustainable exploration of an existing network by shielding it from environmental fluctuations in inputs. Correspondingly, loss of internal controls constrains evolution to the rate of the gains and losses of dietary precursors. Because internalization of a network's controls necessarily bridges diet-specific enzymatic modules within a network, it structurally links local adaptation and continuous evolution even for traits fully dependent on contingent external inputs.

Evolutionary transitions in controls reconcile adaptation with continuity of evolution.

Evolution proceeds by accumulating functional solutions, necessarily forming an uninterrupted lineage from past solutions of ancestors to the current design of extant forms. At the population level, this process requires an organismal architecture in which the maintenance of local adaptation does not preclude the ability to innovate in the same traits and their continuous evolution. Representing complex traits as networks enables us to visualize a fundamental principle that resolves tension between adaptation and continuous evolution: phenotypic states encompassing adaptations traverse the continuous multi-layered landscape of past physical, developmental and functional associations among traits. The key concept that captures such traversing is network controllability - the ability to move a network from one state into another while maintaining its functionality (reflecting evolvability) and to efficiently propagate information or products through the network within a phenotypic state (maintaining its robustness). Here I suggest that transitions in network controllability - specifically in the topology of controls - help to explain how robustness and evolvability are balanced during evolution. I will focus on evolutionary transitions in degeneracy of metabolic networks - a ubiquitous property of phenotypic robustness where distinct pathways achieve the same end product - to suggest that associated changes in network controls is a common rule underlying phenomena as distinct as phenotypic plasticity, organismal accommodation of novelties, genetic assimilation, and macroevolutionary diversification. Capitalizing on well understood principles by which network structure translates into function of control nodes, I show that accumulating redundancy in one type of network controls inevitably leads to the emergence of another type of controls, forming evolutionary cycles of network controllability that, ultimately, reconcile local adaptation with continuity of evolution.

Extensive phenotypic diversification coexists with little genetic divergence and a lack of population structure in the White Wagtail subspecies complex (Motacilla alba).

Geographically clustered phenotypes often demonstrate consistent patterns in molecular markers, particularly mitochondrial DNA (mtDNA) traditionally used in phylogeographic studies. However, distinct evolutionary trajectories among traits and markers can lead to their discordance. First, geographic structure in phenotypic traits and nuclear molecular markers can be co-aligned but inconsistent with mtDNA (mito-nuclear discordance). Alternatively, phenotypic variation can have little to do with patterns in neither mtDNA nor nuclear markers. Disentangling between these distinct patterns can provide insight into the role of selection, demography and gene flow in population divergence. Here, we examined a previously reported case of strong inconsistency between geographic structure in mtDNA and plumage traits in a widespread polytypic bird species, the White Wagtail (Motacilla alba). We tested whether this pattern is due to mito-nuclear discordance or discrepancy between morphological evolution and both nuclear and mtDNA markers. We analysed population differentiation and structure across six out of nine commonly recognized subspecies using 17 microsatellite loci and a combination of microsatellites and plumage indices in a comprehensively sampled region of a contact between two subspecies. We did not find support for the mito-nuclear discordance hypothesis: nuclear markers indicated a subtle signal of genetic clustering only partially consistent with plumage groups, similar to previous findings that relied on mtDNA. We discuss evolutionary factors that could have shaped the intricate patterns of phenotypic diversification in the White wagtail and the role that repeated selection on plumage 'hotspots' and hybridization may have played.

Structure versus time in the evolutionary diversification of avian carotenoid metabolic networks.

Historical associations of genes and proteins are thought to delineate pathways available to subsequent evolution; however, the effects of past functional involvements on contemporary evolution are rarely quantified. Here, we examined the extent to which the structure of a carotenoid enzymatic network persists in avian evolution. Specifically, we tested whether the evolution of carotenoid networks was most concordant with phylogenetically structured expansion from core reactions of common ancestors or with subsampling of biochemical pathway modules from an ancestral network. We compared structural and historical associations in 467 carotenoid networks of extant and ancestral species and uncovered the overwhelming effect of pre-existing metabolic network structure on carotenoid diversification over the last 50 million years of avian evolution. Over evolutionary time, birds repeatedly subsampled and recombined conserved biochemical modules, which likely maintained the overall structure of the carotenoid metabolic network during avian evolution. These findings explain the recurrent convergence of evolutionary distant species in carotenoid metabolism and weak phylogenetic signal in avian carotenoid evolution. Remarkable retention of an ancient metabolic structure throughout extensive and prolonged ecological diversification in avian carotenoid metabolism illustrates a fundamental requirement of organismal evolution - historical continuity of a deterministic network that links past and present functional associations of its components.

Emergent buffering balances evolvability and robustness in the evolution of phenotypic flexibility.

Evolution of adaptive phenotypic flexibility requires a system that can dynamically restore and update a functional phenotype in response to environmental change. The architecture of such a system evolves under the conflicting demands of versatility and robustness, and resolution of these demands should be particularly evident in organisms that require external inputs for reiterative trait production within a generation, such as in metabolic networks that underlie yearly acquisition of diet-dependent coloration in birds. Here, we show that a key structural feature of carotenoid networks-redundancy of biochemical pathways-enables these networks to translate variable environmental inputs into consistent phenotypic outcomes. We closely followed life-long changes in structure and utilization of metabolic networks in a large cohort of free-living birds and found that greater individual experience with dietary change between molts leads to wider occupancy of the metabolic network and progressive accumulation of redundant pathways in a functionally active network. This generated a regime of emergent buffering whereby greater dietary experience was mechanistically linked to greater robustness of resulting traits and an increasing ability to retain and implement previous adaptive solutions. Thus, experience-related buffering links evolvability and robustness in carotenoid-metabolizing networks and we argue that this mechanistic principle facilitates the evolution of phenotypic flexibility.

Most Colorful Example of Genetic Assimilation? Exploring the Evolutionary Destiny of Recurrent Phenotypic Accommodation.

Evolution of adaptation requires both generation of novel phenotypic variation and retention of a locally beneficial subset of this variation. Such retention can be facilitated by genetic assimilation, the accumulation of genetic and molecular mechanisms that stabilize induced phenotypes and assume progressively greater control over their reliable production. A particularly strong inference into genetic assimilation as an evolutionary process requires a system where it is possible to directly evaluate the extent to which an induced phenotype is progressively incorporated into preexisting developmental pathways. Evolution of diet-dependent pigmentation in birds-where external carotenoids are coopted into internal metabolism to a variable degree before being integrated with a feather's developmental processes-provides such an opportunity. Here we combine a metabolic network view of carotenoid evolution with detailed empirical study of feather modifications to show that the effect of physical properties of carotenoids on feather structure depends on their metabolic modification, their environmental recurrence, and biochemical redundancy, as predicted by the genetic assimilation hypothesis. Metabolized carotenoids caused less stochastic variation in feather structure and were more closely integrated with feather growth than were dietary carotenoids of the same molecular weight. These patterns were driven by the recurrence of organism-carotenoid associations: commonly used dietary carotenoids and biochemically redundant derived carotenoids caused less stochastic variation in feather structure than did rarely used or biochemically unique compounds. We discuss implications of genetic assimilation processes for the evolutionary diversification of diet-dependent animal coloration.

Structuring evolution: biochemical networks and metabolic diversification in birds.

BACKGROUND: Recurrence and predictability of evolution are thought to reflect the correspondence between genomic and phenotypic dimensions of organisms, and the connectivity in deterministic networks within these dimensions. Direct examination of the correspondence between opportunities for diversification imbedded in such networks and realized diversity is illuminating, but is empirically challenging because both the deterministic networks and phenotypic diversity are modified in the course of evolution. Here we overcome this problem by directly comparing the structure of a "global" carotenoid network - comprising of all known enzymatic reactions among naturally occurring carotenoids - with the patterns of evolutionary diversification in carotenoid-producing metabolic networks utilized by birds. RESULTS: We found that phenotypic diversification in carotenoid networks across 250 species was closely associated with enzymatic connectivity of the underlying biochemical network - compounds with greater connectivity occurred the most frequently across species and were the hotspots of metabolic pathway diversification. In contrast, we found no evidence for diversification along the metabolic pathways, corroborating findings that the utilization of the global carotenoid network was not strongly influenced by history in avian evolution. CONCLUSIONS: The finding that the diversification in species-specific carotenoid networks is qualitatively predictable from the connectivity of the underlying enzymatic network points to significant structural determinism in phenotypic evolution.

The Landscape of Evolution: Reconciling Structural and Dynamic Properties of Metabolic Networks in Adaptive Diversifications.

The network of the interactions among genes, proteins, and metabolites delineates a range of potential phenotypic diversifications in a lineage, and realized phenotypic changes are the result of differences in the dynamics of the expression of the elements and interactions in this deterministic network. Regulatory mechanisms, such as hormones, mediate the relationship between the structural and dynamic properties of networks by determining how and when the elements are expressed and form a functional unit or state. Changes in regulatory mechanisms lead to variable expression of functional states of a network within and among generations. Functional properties of network elements, and the magnitude and direction of evolutionary change they determine, depend on their location within a network. Here, we examine the relationship between network structure and the dynamic mechanisms that regulate flux through a metabolic network. We review the mechanisms that control metabolic flux in enzymatic reactions and examine structural properties of the network locations that are targets of flux control. We aim to establish a predictive framework to test the contributions of structural and dynamic properties of deterministic networks to evolutionary diversifications.

Evolution of long-term coloration trends with biochemically unstable ingredients.

The evolutionarily persistent and widespread use of carotenoid pigments in animal coloration contrasts with their biochemical instability. Consequently, evolution of carotenoid-based displays should include mechanisms to accommodate or limit pigment degradation. In birds, this could involve two strategies: (i) evolution of a moult immediately prior to the mating season, enabling the use of particularly fast-degrading carotenoids and (ii) evolution of the ability to stabilize dietary carotenoids through metabolic modification or association with feather keratins. Here, we examine evolutionary lability and transitions between the two strategies across 126 species of birds. We report that species that express mostly unmodified, fast-degrading, carotenoids have pre-breeding moults, and a particularly short time between carotenoid deposition and the subsequent breeding season. Species that expressed mostly slow-degrading carotenoids in their plumage accomplished this through increased metabolic modification of dietary carotenoids, and the selective expression of these slow-degrading compounds. In these species, the timing of moult was not associated with carotenoid composition of plumage displays. Using repeated samples from individuals of one species, we found that metabolic modification of dietary carotenoids significantly slowed their degradation between moult and breeding season. Thus, the most complex and colourful ornamentation is likely the most biochemically stable in birds, and depends less on ecological factors, such as moult timing and migration tendency. We suggest that coevolution of metabolic modification, selective expression and biochemical stability of plumage carotenoids enables the use of unstable pigments in long-term evolutionary trends in plumage coloration.

Causes of Discordance between Allometries at and above Species Level: An Example with Aquatic Beetles.

Covariation among organismal traits is nearly universal, occurring both within and among species (static and evolutionary allometry, respectively). If conserved developmental processes produce similarity in static and evolutionary allometry, then when species differ in development, it should be expressed in discordance between allometries. Here, we investigate whether rapidly evolving developmental processes result in discordant static and evolutionary allometries attributable to trade-offs in resource acquisition, allocation, or growth across 30 species of aquatic beetles. The highly divergent sperm phenotypes of these beetles might be an important contributor to allometric evolution of testis and accessory gland mass through altered requirements for the production of sperm and seminal fluids. We documented extensive discordance between static and evolutionary allometries, indicating that allometric relationships are flexibly modified over short time periods but subject to constraint over longer time spans. Among species, sperm phenotype did not influence relative investment in accessory glands but was weakly associated with investment in testes. Furthermore, except when sperm were long and simple, sperm phenotype was not associated with species-specific modification of the allometry of testis/accessory gland mass and body size. Our results demonstrate the utility of allometric discordance to infer species differences in the provisioning and growth of concurrently developing traits.

Tradeoff between robustness and elaboration in carotenoid networks produces cycles of avian color diversification.

BACKGROUND: Resolution of the link between micro- and macroevolution calls for comparing both processes on the same deterministic landscape, such as genomic, metabolic or fitness networks. We apply this perspective to the evolution of carotenoid pigmentation that produces spectacular diversity in avian colors and show that basic structural properties of the underlying carotenoid metabolic network are reflected in global patterns of elaboration and diversification in color displays. Birds color themselves by consuming and metabolizing several dietary carotenoids from the environment. Such fundamental dependency on the most upstream external compounds should intrinsically constrain sustained evolutionary elongation of multi-step metabolic pathways needed for color elaboration unless the metabolic network gains robustness - the ability to synthesize the same carotenoid from an additional dietary starting point. RESULTS: We found that gains and losses of metabolic robustness were associated with evolutionary cycles of elaboration and stasis in expressed carotenoids in birds. Lack of metabolic robustness constrained lineage's metabolic explorations to the immediate biochemical vicinity of their ecologically distinct dietary carotenoids, whereas gains of robustness repeatedly resulted in sustained elongation of metabolic pathways on evolutionary time scales and corresponding color elaboration. CONCLUSIONS: The structural link between length and robustness in metabolic pathways may explain periodic convergence of phylogenetically distant and ecologically distinct species in expressed carotenoid pigmentation; account for stasis in carotenoid colors in some ecological lineages; and show how the connectivity of the underlying metabolic network provides a mechanistic link between microevolutionary elaboration and macroevolutionary diversification.

Epigenetic resolution of the 'curse of complexity' in adaptive evolution of complex traits.

The age of most genes exceeds the longevity of their genomic and physiological associations by many orders of magnitude. Such transient contexts modulate the expression of ancient genes to produce currently appropriate and often highly distinct developmental and functional outcomes. The efficacy of such adaptive modulation is diminished by the high dimensionality of complex organisms and associated vast areas of neutrality in their genotypic and developmental networks (and, thus, weak natural selection). Here I explore whether epigenetic effects facilitate adaptive modulation of complex phenotypes by effectively reducing the dimensionality of their deterministic networks and thus delineating their developmental and evolutionary trajectories even under weak selection. Epigenetic effects that link unconnected or widely dispersed elements of genotype space in ecologically relevant time could account for the rapid appearance of functionally integrated adaptive modifications. On an organismal time scale, conceptually similar processes occur during recurrent epigenetic reprogramming of somatic stem cells to produce, recurrently and reversibly, a bewildering array of differentiated and persistent cell lineages, all sharing identical genomic sequences despite strongly distinct phenotypes. I discuss whether close dependency of onset, scope and duration of epigenetic effects on cellular and genomic context in stem cells could provide insights into contingent modulation of conserved genomic material on a much longer evolutionary time scale. I review potential empirical examples of epigenetic bridges that reduce phenotype dimensionality and accomplish rapid adaptive modulation in the evolution of novelties, expression of behavioural types, and stress-induced ossification schedules.

"Homeostatic hitchhiking": a mechanism for the evolutionary retention of complex adaptations.

The complexity of organismal organization channels and accommodates novel genomic and developmental modifications. Here, I extend this perspective to suggest that emergent processes that dominate homeostasis-co-option, re-use, and recombination of accumulated elements-can create configurations and dependencies among these elements that strongly reduce the number of evolutionary steps needed for the evolution of precise novel adaptations. Evolutionary retention and environmental matching of such configurations are further facilitated when they include elements of homeostasis that are responsive to particular environmental cues. I apply this perspective to the study of evolution of sex-biased egg-laying in birds, a phenomenon that combines precision, complexity, context-dependency, and reversibility. I show that homeostatic hitchhiking can overcome the main difficulty in the evolution of this adaptation-the perceived necessity of de novo co-evolution of oogenesis, sex-determination, and order of ovulation in each environmental context-something that would require unrealistic expectations of evolutionary rates and population sizes and is not a desirable outcome for a process that needs to retain substantial environmental sensitivity. First, I explain the rationale behind the homeostatic-hitchhiking hypothesis and outline its predictions specifically for studies of sex-bias in order of egg-laying. Second, I show that a combination of self-regulatory and emergent processes and ubiquitous re-use of conserved growth factors make oogenesis particularly amendable to homeostatic hitchhiking. Third, I review empirical evidence for this mechanism in the rapid evolution of adaptive sex-biased order of egg-laying that accompanied colonization of North America by the house finch (Carpodacus mexicanus).

Gene loss, thermogenesis, and the origin of birds.

Compared to related taxa, birds have exceptionally enlarged and diversified skeletal muscles, features that are closely associated with skeletal diversification and are commonly explained by a diversity of avian ecological niches and locomotion types. The thermogenic muscle hypothesis (TMH) for the origin of birds proposes that such muscle hyperplasia and the associated skeletal innovations are instead the consequence of the avian clade originating from an ancestral population that underwent several successive episodes of loss of genes associated with thermogenesis, myogenesis, and skeletogenesis. Direct bird ancestors met this challenge with a combination of behavioral strategies (e.g., brooding of nestlings) and acquisition of a variety of adaptations for enhanced nonshivering thermogenesis in skeletal muscle. The latter include specific biochemical alterations promoting muscle heat generation and dramatic expansion of thigh and breast muscle mass. The TMH proposes that such muscle hyperplasia facilitated bipedality, freeing upper limbs for new functions (e.g., flight, swimming), and, by altering the mechanical environment of embryonic development, generated skeletal novelties, sometimes abruptly, that became distinctive features of the avian body plan.

Developmental integration of feather growth and pigmentation and its implications for the evolution of diet-derived coloration.

Variation in avian coloration is produced by coordinated pigmentation of thousands of growing feathers that vary in shape and size. Although the functional consequences of avian coloration are frequently studied, little is known about its developmental basis, and, specifically, the rules that link feather growth to pigment uptake and synthesis. Here, we combine biochemical, modeling, and morphometric techniques to examine the developmental basis of feather pigmentation in house finches (Carpodacus mexicanus)--a species with extensive variation in both growth dynamics of ornamental feathers and their carotenoid pigmentation. We found that the rate of carotenoid uptake was constant across a wide range of feather sizes and shapes, and the relative pigmented area of feathers was independent of the total amount of deposited carotenoids. Analysis of the developmental linkage of feather growth and pigment uptake showed that the mechanisms behind partitioning the feather into pigmented and nonpigmented parts and the mechanisms regulating carotenoid uptake into growing feathers are partially independent. Carotenoid uptake strongly covaried with early elements of feather differentiation (the barb addition rate and diameter), whereas the pigmented area was most closely associated with the rate of feather growth. We suggest that strong effects of carotenoid uptake on genetically integrated mechanisms of feather growth and differentiation provide a likely route for genetic assimilation of diet-dependent coloration.

Origin of the fittest: link between emergent variation and evolutionary change as a critical question in evolutionary biology.

In complex organisms, neutral evolution of genomic architecture, associated compensatory interactions in protein networks and emergent developmental processes can delineate the directions of evolutionary change, including the opportunity for natural selection. These effects are reflected in the evolution of developmental programmes that link genomic architecture with a corresponding functioning phenotype. Two recent findings call for closer examination of the rules by which these links are constructed. First is the realization that high dimensionality of genotypes and emergent properties of autonomous developmental processes (such as capacity for self-organization) result in the vast areas of fitness neutrality at both the phenotypic and genetic levels. Second is the ubiquity of context- and taxa-specific regulation of deeply conserved gene networks, such that exceptional phenotypic diversification coexists with remarkably conserved generative processes. Establishing the causal reciprocal links between ongoing neutral expansion of genomic architecture, emergent features of organisms' functionality, and often precisely adaptive phenotypic diversification therefore becomes an important goal of evolutionary biology and is the latest reincarnation of the search for a framework that links development, functioning and evolution of phenotypes. Here I examine, in the light of recent empirical advances, two evolutionary concepts that are central to this framework-natural selection and inheritance-the general rules by which they become associated with emergent developmental and homeostatic processes and the role that they play in descent with modification.

Developmental plasticity links local adaptation and evolutionary diversification in foraging morphology.

Developmental plasticity is thought to reconcile the constraining role of natural selection in maintaining local adaptation with evolutionary diversification under novel conditions, but empirical documentations are rare. In vertebrates, growth and development of bones is partially guided by contractions of attached musculature and such muscle activity changes progressively through embryonic development from sporadic motility to direct functional effects. In species with short generation times, delayed skull maturation extends the guiding effects of muscle activity on formation of foraging morphology into adulthood, providing an opportunity to directly examine the links between plasticity of bone development, ecological adaptations, and evolutionary diversification in foraging morphology. In this case, the morphological consequences of inputs due to local functional requirements should be evident in adaptive divergence across taxa. Here we provide evidence that epigenetic regulation of bone growth in Soricid shrews may enable both development of local adaptations and evolutionary divergence in mandibular morphology. We contrast the effects of muscle stimulation on early- vs. late-maturing components of, foraging apparatus to show that the morphology of late-maturing components is more affected by functional requirements than are early-ossifying traits. Further, the divergence in foraging morphology across shrew species occurs along the directions delineated by inductive effects of muscle loading and bite force on bone formation in late-maturing but not early-maturing mandible components within species. These results support the hypothesis that developmental plasticity can link maintenance of local adaptations with evolutionary diversification in morphology.

Structure of social networks in a passerine bird: consequences for sexual selection and the evolution of mating strategies.

The social environment is a critical determinant of fitness and, in many taxa, is shaped by an individual's behavioral discrimination among social contexts, suggesting that animals can actively influence the selection they experience. In competition to attract females, males may modify sexual selection by choosing social environments in which they are more attractive relative to rivals. Across the population, such behaviors should influence sexual selection patterns by altering the relationship between male mating success and sexual ornament elaboration. Here we use network analysis to examine patterns of male social behavior in relation to plumage ornamentation and mating success in a free-living population of house finches. During the nonbreeding season, less elaborate males changed associations with distinct social groups more frequently, compared to more elaborate males that showed greater fidelity to a single social group. By the onset of pair formation, socially labile males effectively increased their attractiveness relative to other males in the same flocks. Consequently, males that frequently moved between social groups had greater pairing success than less social individuals with equivalent sexual ornamentation. We discuss these results in relation to conditional mating tactics and the role of social behavior in evolutionary change by sexual selection.

The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution.

The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak's precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies-a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis-beak depth-was mirrored in the structure of beak's additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution.