skip to main content


Title: Postnatal expression of IGF2 is the norm in amniote vertebrates
The insulin and insulin-like signalling (IIS) network plays an important role in mediating several life-history traits, including growth, reproduction and senescence. Although insulin-like growth factors (IGFs) 1 and 2 are both key hormones in the vertebrate IIS network, research on IGF2 in juveniles and adults has been largely neglected because early biomedical research on rodents found negligible IGF2 postnatal expression. Here, we challenge this assumption and ask to what degree IGF2 is expressed during postnatal life across amniotes by quantifying the relative gene expression of IGF1 and IGF2 using publicly available RNAseq data for 82 amniote species and quantitative polymerase chain reaction on liver cDNA at embryonic, juvenile and adult stages for two lizard, bird and mouse species. We found that (i) IGF2 is expressed postnatally across amniote species and life stages—often at a higher relative expression than IGF1 , contradicting rodent models; (ii) the lack of rodent postnatal IGF2 expression is due to phylogenetic placement, not inbreeding or artificial selection; and (iii) adult IGF2 expression is sex-biased in some species. Our results demonstrate that IGF2 expression is typical for amniotes throughout life, suggesting that a comprehensive understanding of the mechanisms mediating variation in life-history traits will require studies that measure both IGFs.  more » « less
Award ID(s):
1845974
NSF-PAR ID:
10333915
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
289
Issue:
1969
ISSN:
0962-8452
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Synopsis

    Sexual size dimorphism is widespread in nature and often develops through sexual divergence in growth trajectories. In vertebrates, the growth hormone/insulin-like growth factor (GH/IGF) network is an important regulator of growth, and components of this network are often regulated in sex-specific fashion during the development of sexual size dimorphism. However, expression of the GH/IGF network is not well characterized outside of mammalian model systems, and the extent to which species differences in sexual size dimorphism are related to differences in GH/IGF network expression is unclear. To begin bridging this gap, we compared GH/IGF network expression in liver and muscle from 2 lizard congeners, one with extreme male-biased sexual size dimorphism (brown anole, Anolis sagrei), and one that is sexually monomorphic in size (slender anole, A. apletophallus). Specifically, we tested whether GH/IGF network expression in adult slender anoles resembles the highly sex-biased expression observed in adult brown anoles or the relatively unbiased expression observed in juvenile brown anoles. We found that adults of the 2 species differed significantly in the strength of sex-biased expression for several key upstream genes in the GH/IGF network, including insulin-like growth factors 1 and 2. However, species differences in sex-biased expression were minor when comparing adult slender anoles to juvenile brown anoles. Moreover, the multivariate expression of the entire GH/IGF network (as represented by the first two principal components describing network expression) was sex-biased for the liver and muscle of adult brown anoles, but not for either tissue in juvenile brown anoles or adult slender anoles. Our work suggests that species differences in sex-biased expression of genes in the GH/IGF network (particularly in the liver) may contribute to the evolution of species differences in sexual size dimorphism.

     
    more » « less
  2. Abstract

    The diversification of many lineages throughout natural history has frequently been associated with evolutionary changes in life cycle complexity. However, our understanding of the processes that facilitate differentiation in the morphologies and functions expressed by organisms throughout their life cycles is limited. Theory suggests that the expression of traits is decoupled across life stages, thus allowing for their evolutionary independence. Although trait decoupling between stages is well established, explanations of how said decoupling evolves have seldom been considered. Because the different phenotypes expressed by organisms throughout their life cycles are coded for by the same genome, trait decoupling must be mediated through divergence in gene expression between stages. Gene duplication has been identified as an important mechanism that enables divergence in gene function and expression between cells and tissues. Because stage transitions across life cycles require changes in tissue types and functions, we investigated the potential link between gene duplication and expression divergence between life stages. To explore this idea, we examined the temporal changes in gene expression across the monarch butterfly (Danaus plexippus) metamorphosis. We found that within homologous groups, more phylogenetically diverged genes exhibited more distinct temporal expression patterns. This relationship scaled such that more phylogenetically diverse homologous groups showed more diverse patterns of gene expression. Furthermore, we found that duplicate genes showed increased stage-specificity relative to singleton genes. Overall, our findings suggest an important link between gene duplication and the evolution of complex life cycles.

     
    more » « less
  3. null (Ed.)
    ABSTRACT Metabolism is thought to mediate the connection between environmental selection pressures and a broad array of life history tradeoffs, but tests are needed. High juvenile predation correlates with fast growth, which may be achieved via fast juvenile metabolism. Fast offspring metabolism and growth can create physiological costs later in life that should be minimized in species with low adult mortality. Yet, relationships between juvenile metabolism and mortality at offspring versus adult stages are unexplored. We found that post-natal metabolism was positively correlated with adult mortality but not nest predation rates among 43 songbird species on three continents. Nest predation, but not adult mortality, explained additional variation in growth rates beyond metabolism. Our results suggest that metabolism may not be the mechanism underlying the relationships between growth and mortality at different life stages. 
    more » « less
  4. Climate change is shifting the phenological timing, duration, and temporal overlap of interacting species in natural communities, reshaping temporal interaction networks worldwide. Despite much recent progress in documenting these phenological shifts, little is known about how the phenologies of species interactions are tracked across different life history stages. Here we analyze four key phenological traits and the pairwise interaction potential of nine amphibian species for the adult (calling/breeding) and subsequent larval (tadpole) stage at eight different sites over six years. We found few strong correlations among phenological traits within species, but the strength of these correlations varied across species. As a consequence, phenological trait combinations of both stages varied substantially across species without clear signs of multidimensional clustering, indicating a distinct and diverse range of species‐specific phenological strategies. Despite this considerable variation in the phenologies across species, the temporal overlap between species was largely preserved through the two life history stages. Further, we also detected significant correlations among the duration and temporal overlap of interactions with other species across stages in five species, demonstrating that temporal patterns of species interactions are mirrored across life history stages. For these species, these results indicate a strong tracking of phenologies and species interactions across life history stages even in species with complex life cycles where stages occupy completely different environments. This suggests that phenological shifts in one stage can impact the temporal dynamics and structure of interaction networks across developmental stages.

     
    more » « less
  5. Synopsis

    Climate resilience, a focus of many recent studies, has been examined from ecological, physiological, and evolutionary perspectives. However, sampling biases toward adults, males, and certain species have made establishing the link between environmental change and population-level change problematic. Here, we used data from four laboratory studies, in which we administered pre- and postnatal stressors, such as suboptimal incubation temperature, heat stress, and food restriction, to zebra finches. We then quantified hatching success, posthatch survival, and reproductive success, to parameterize age-structured population dynamics models with the goal of estimating the effect of the stressors on relative population growth rates. Using the same model structure, we tested the hypothesis that early life stages influence population growth rate more than later life stages. Our models suggested that stressful events during embryonic development, such as suboptimal incubation temperatures and reduced gas exchange for the embryos, have a greater total impact on population growth than posthatch stressors, such as heat stress and food restriction. However, among life history traits, differences in hatching success and sex ratio of offspring in response to stressors changed population growth rates more than differences in any other demographic rate estimates. These results suggest that when predicting population resilience against climate change, it is critical to account for effects of climate change on all life stages, including early stages of life, and to incorporate individuals’ physiology and stress tolerance that likely influence future stress responses, reproduction, and survival.

     
    more » « less