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

Habitat Sampling and Habitat Selection by Female Wild Turkeys: Ecological Correlates and Reproductive Consequences

Habitat sampling can allow much more effective habitat selection for longterm activities such as nesting and may be directly linked to fitness. We studied the process of habitat sampling and selection in female Wild Turkeys (Meleagris gallopavo) in the Arkansas Ozarks. In particular, we tested the prediction that movements prior to selecting nesting habitat correlate with the quality of selected habitat. Our results supported the prediction that greater habitat sampling (as reflected by greater area covered prior to nesting) allows acquisition of better nesting habitat; greater movements were correlated with choice of better nesting sites with more cover that allow higher nest survival. Attributes of individual birds and habitat dispersion influenced movement patterns and access to quality habitats. In addition, extent of habitat sampling early in the season correlated with reproductive performance by affecting renesting. Distance between subsequent nest locations was inversely related to the movements early in the season and also depended upon length of incubation before nest predation. Females that sampled larger areas after depredation of their first nest and did so outside of their prenesting range were more successful than other females

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

Curse of the black spot: spotting negatively correlate with fitness in black grouse Lyrurus tetrix

There is growing evidence that achromatic plumage can act as honest indicators of male quality. In some species with areas of white plumage, black melanin spots can be found on parts of the feathers. The functional significance of these spots and the relationship with male quality is yet poorly understood. We investigated the relationship between black melanin spots in an otherwise totally white ornament, the undertail covert, in relation to age, fitness and covariance with past and present expression of sexual traits, in the lekking black grouse Lyrurus tetrix. We found that spots at tips of feathers (tip spots) were negatively related to survival and reproductive success, and covaried negatively with current fighting rate. They also covaried positively with past fighting rate, suggesting high investment in fighting leads to carryover effects on male condition. In contrast, spots found further down the feather (vane spots) were unrelated to fitness and morphological and behavioural trait expression. Our results show that melanin spots can indicate some relationship with male quality and that the location of the spots has some importance in this relationship. However, the exact drivers of melanin spot expression and how these link to male quality, are currently unknown

Progressive, Transgenerational Changes in Offspring Phenotype and Epigenotype following Nutritional Transition

Induction of altered phenotypes during development in response to environmental input involves epigenetic changes. Phenotypic traits can be passed between generations by a variety of mechanisms, including direct transmission of epigenetic states or by induction of epigenetic marks de novo in each generation. To distinguish between these possibilities we measured epigenetic marks over four generations in rats exposed to a sustained environmental challenge. Dietary energy was increased by 25% at conception in F0 female rats and maintained at this level to generation F3. F0 dams showed higher pregnancy weight gain, but lower weight gain and food intake during lactation than F1 and F2 dams. On gestational day 8, fasting plasma glucose concentration was higher and β-hydroxybutyrate lower in F0 and F1 dams than F2 dams. This was accompanied by decreased phosphoenolpyruvate carboxykinase (PEPCK) and increased PPARα and carnitine palmitoyl transferase-1 mRNA expression. PEPCK mRNA expression was inversely related to the methylation of specific CpG dinucleotides in its promoter. DNA methyltransferase (Dnmt) 3a2, but not Dnmt1 or Dnmt3b, expression increased and methylation of its promoter decreased from F1 to F3 generations. These data suggest that the regulation of energy metabolism during pregnancy and lactation within a generation is influenced by the maternal phenotype in the preceding generation and the environment during the current pregnancy. The transgenerational effects on phenotype were associated with altered DNA methylation of specific genes in a manner consistent with induction de novo of epigenetic marks in each generation