Environmental induction and phenotypic retention of adaptive maternal effects

<p>Abstract</p> <p>Background</p> <p>The origin of complex adaptations is one of the most controversial questions in biology. Environmental induction of novel phenotypes, where phenotypic retention of adaptive developmental variation is enabled by organismal complexity and homeostasis, can be a starting point in the evolution of some adaptations, but empirical examples are rare. Comparisons of populations that differ in historical recurrence of environmental induction can offer insight into its evolutionary significance, and recent colonization of North America by the house finch (<it>Carpodacus mexicanus</it>) provides such an opportunity.</p> <p>Results</p> <p>In both native (southern Arizona) and newly established (northern Montana, 18 generations) populations, breeding female finches exhibit the same complex adaptation – a sex-bias in ovulation sequence – in response to population-specific environmental stimulus of differing recurrence. We document that, in the new population, the adaptation is induced by a novel environment during females' first breeding and is subsequently retained across breeding attempts. In the native population, first-breeding females expressed a precise adaptive response to a recurrent environmental stimulus without environmental induction. We document strong selection on environmental cue recognition in both populations and find that rearrangement of the same proximate mechanism – clustering of oocytes that become males and females – can enable an adaptive response to distinct environmental stimuli.</p> <p>Conclusion</p> <p>The results show that developmental plasticity induced by novel environmental conditions confers significant fitness advantages to both maternal and offspring generations and might play an important role not only in the successful establishment of this invasive species across the widest ecological range of extant birds, but also can link environmental induction and genetic inheritance in the evolution of novel adaptations.</p

Evolution of Morphological Integration. I. Functional Units Channel Stress-Induced Variation in Shrew Mandibles

Stress-induced deviations from normal development are often assumed to be random, yet their accumulation and expression can be influenced by patterns of morphological integration within an organism. We studied within-individual developmental variation ( fluctuating asymmetry) in the mandible of four shrew species raised under normal and extreme environments. Patterns of among-individual variation and fluctuating asymmetry were strongly concordant in traits that were involved in the attachment of the same muscles (i.e., functionally integrated traits), and fluctuating asymmetry was closely integrated among these traits, implying direct developmental interactions among traits involved in the same function. Stress-induced variation was largely confined to the directions delimited by functionally integrated groups of traits in the pattern that was concordant with species divergence-species differed most in the same traits that were most sensitive to stress within each species. These results reveal a strong effect of functional complexes on directing and incorporating stress-induced variation during development and might explain the historical persistence of sets of traits involved in the same function in shrew jaws despite their high sensitivity to environmental variation

Stress and Developmental Stability: Vegetation Removal Causes Increased Fluctuating Asymmetry in Shrews

Environmental stress can increase phenotypic variation in populations by affecting developmental stability of individuals. While such increase in variation results from individual differences in ability to buffer stress, groups of individuals and different traits may have different sensitivity to stressful conditions. For example, the sex that is under stronger directional selection for faster growth may be more sensitive to stressful conditions during development. On an individual level, stress-induced variation in a trait may be related to the strength of stabilizing selection that acts on the trait. We experimentally examined sensitivity of mandibular development to stress in a free-living population of common shrews (Sorex cinereus), a short-lived insectivore mammal with very limited dispersal and nearly continuous foraging activity. We found a strong increase in asymmetry in shrews born under stressful conditions. Increased asymmetry was associated with lower physiological condition in both control and stressed populations, although the effect of asymmetry on fitness was more pronounced under stressful conditions. Males\u27 developmental stability was more sensitive to stressful conditions than developmental stability of females, suggesting that their apparently faster and more variable growth is more sensitive to stress than is growth of females. Mandible traits differed in their sensitivity to environmental changes. Preliminary results suggest that this differential sensitivity is proportional to the degree of developmental and functional morphological integration among mandibular traits

Evolution of Morphological Integration: Developmental Accommodation of Stress-Induced Variation

Extreme environmental change during growth often results in an increase in developmental abnormalities in the morphology of an organism. The evolutionary significance of such stress-induced variation depends on the recurrence of a stressor and on the degree to which developmental errors can be accommodated by an organism\u27s ontogeny without significant loss of function. We subjected populations of four species of soricid shrews to an extreme environment during growth and measured changes in the patterns of integration and accommodation of stress-induced developmental errors in a complex of mandibular traits. Adults that grew under an extreme environment had lower integration of morphological variation among mandibular traits and highly elevated fluctuating asymmetry in these traits, compared to individuals that grew under the control conditions. However, traits differed strongly in the magnitude of response to a stressor - traits within attachments of the same muscle (functionally integrated traits) had lower response and changed their integration less than other traits. Cohesiveness in functionally integrated complexes of traits under stress was maintained by close covariation of their developmental variation. Such developmental accommodation of stress-induced variation might enable the individual\u27s functioning and persistence under extreme environmental conditions and thus provides a link between individual adaptation to stress and the evolution of stress resistance

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. REVIEWERS: This article was reviewed by Junhyong Kim, Eugene Koonin, and Fyodor Kondrashov. For complete reports, see the Reviewers' reports section.This item is part of the UA Faculty Publications collection. For more information this item or other items in the UA Campus Repository, contact the University of Arizona Libraries at [email protected]

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.David and Lucille Packard Foundation, Amherst College graduate fellowshipsOpen access.This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]

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.National Science Foundation; Packard Foundation Fellowship; Galileo Fellowship12 month embargo; Published online: 15 May 2017This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at [email protected]