Evolution of regulatory mechanisms underlying nutrition-responsive plasticity in insects

Phenotypic plasticity is a fundamental property of developing organisms and is thought to play an important role in diversification. Plastic responses themselves are remarkably diverse and respond to a wide range of environmental factors. Here I focus on plasticity in response to variation in nutrition in insects since 1) nutrition is a widespread factor that impacts most organisms, and 2) insects are important models to study phenotypic plasticity. First, I provide a brief overview of our current mechanistic understanding of the regulation of nutritionally cued plasticity in insects, in both traditional as well as emerging model systems. Then, I explore evolutionary mechanisms enabling the diversification of regulation across taxa, emphasizing the role of gene duplication and gene regulatory network co-option. Furthermore, I examine nutrition-responsive phenotypes as suites of multiple traits that develop in a coordinated manner. I argue that understanding how these traits are integrated at the molecular level can shed light on the evolution of complex phenotypes. Finally, I discuss potential challenges and opportunities to further our understanding of nutrition-responsive plasticity, its regulation, and its evolution

On the Reciprocally Causal and Constructive Nature of Developmental Plasticity and Robustness

Exposure to environmental variation is a characteristic feature of normal development, one that organisms can respond to during their lifetimes by actively adjusting or maintaining their phenotype in order to maximize fitness. Plasticity and robustness have historically been studied by evolutionary biologists through quantitative genetic and reaction norm approaches, while more recent efforts emerging from evolutionary developmental biology have begun to characterize the molecular and developmental genetic underpinnings of both plastic and robust trait formation. In this review, we explore how our growing mechanistic understanding of plasticity and robustness is beginning to force a revision of our perception of both phenomena, away from our conventional view of plasticity and robustness as opposites along a continuum and toward a framework that emphasizes their reciprocal, constructive, and integrative nature. We do so in three sections. Following an introduction, the first section looks inward and reviews the genetic, epigenetic, and developmental mechanisms that enable organisms to sense and respond to environmental conditions, maintaining and adjusting trait formation in the process. In the second section, we change perspective and look outward, exploring the ways in which organisms reciprocally shape their environments in ways that influence trait formation, and do so through the lens of behavioral plasticity, niche construction, and host–microbiota interactions. In the final section, we revisit established plasticity and robustness concepts in light of these findings, and highlight research opportunities to further advance our understanding of the causes, mechanisms, and consequences of these ubiquitous, and interrelated, phenomena

The sequencing and interpretation of the genome obtained from a Serbian individual

Recent genetic studies and whole-genome sequencing projects have greatly improved our understanding of human variation and clinically actionable genetic information. Smaller ethnic populations, however, remain underrepresented in both individual and large-scale sequencing efforts and hence present an opportunity to discover new variants of biomedical and demographic significance. This report describes the sequencing and analysis of a genome obtained from an individual of Serbian origin, introducing tens of thousands of previously unknown variants to the currently available pool. Ancestry analysis places this individual in close proximity of the Central and Eastern European populations; i.e., closest to Croatian, Bulgarian and Hungarian individuals and, in terms of other Europeans, furthest from Ashkenazi Jewish, Spanish, Sicilian, and Baltic individuals. Our analysis confirmed gene flow between Neanderthal and ancestral pan-European populations, with similar contributions to the Serbian genome as those observed in other European groups. Finally, to assess the burden of potentially disease-causing/clinically relevant variation in the sequenced genome, we utilized manually curated genotype-phenotype association databases and variant-effect predictors. We identified several variants that have previously been associated with severe early-onset disease that is not evident in the proband, as well as variants that could yet prove to be clinically relevant to the proband over the next decades. The presence of numerous private and low-frequency variants along with the observed and predicted disease-causing mutations in this genome exemplify some of the global challenges of genome interpretation, especially in the context of understudied ethnic groups.Comment: 18 pages, 2 figure

The sequencing and interpretation of the genome obtained from a Serbian individual

Recent genetic studies and whole-genome sequencing projects have greatly improved our understanding of human variation and clinically actionable genetic information. Smaller ethnic populations, however, remain underrepresented in both individual and large-scale sequencing efforts and hence present an opportunity to discover new variants of biomedical and demographic significance. This report describes the sequencing and analysis of a genome obtained from an individual of Serbian origin, introducing tens of thousands of previously unknown variants to the currently available pool. Ancestry analysis places this individual in close proximity to Central and Eastern European populations; i.e., closest to Croatian, Bulgarian and Hungarian individuals and, in terms of other Europeans, furthest from Ashkenazi Jewish, Spanish, Sicilian and Baltic individuals. Our analysis confirmed gene flow between Neanderthal and ancestral pan-European populations, with similar contributions to the Serbian genome as those observed in other European groups. Finally, to assess the burden of potentially disease-causing/clinically relevant variation in the sequenced genome, we utilized manually curated genotype-phenotype association databases and variant-effect predictors. We identified several variants that have previously been associated with severe early-onset disease that is not evident in the proband, as well as putatively impactful variants that could yet prove to be clinically relevant to the proband over the next decades. The presence of numerous private and low-frequency variants, along with the observed and predicted disease-causing mutations in this genome, exemplify some of the global challenges of genome interpretation, especially in the context of under-studied ethnic groups

Data from: Insulin signaling’s role in mediating tissue-specific nutritional plasticity and robustness in the horn-polyphenic beetle Onthophagus taurus

Organisms cope with nutritional variation via developmental plasticity, adjusting trait size to nutrient availability for some traits while enabling others to develop in a nutritionally robust manner. Yet, the developmental mechanisms that regulate organ-specific growth across nutritional gradients remain poorly understood. We assessed the functions of members of the insulin/insulin-like signaling pathway (IIS) in the regulation of nutrition sensitivity and robustness in males of the horn-polyphenic beetle Onthophagus taurus, as well as potential regulatory interactions between IIS and two other growth-regulating pathways: Doublesex and Hedgehog signaling. Using RNA interference (RNAi) we experimentally knocked down both insulin receptors (InR1, InR2) and Foxo, a growth inhibitor. We then performed morphometric measurements on horns, a highly nutrition-sensitive trait, and genitalia, a largely nutrition-insensitive trait. Finally, we used qRT-PCR to assess expression levels of Doublesex and the Hedgehog-signaling gene smoothened following IIS-RNAi. Our results suggest that nutrition responsiveness of both traits is regulated by different IIS components, which transduce nutritional conditions to both Doublesex and Hedgehog pathways, albeit via different IIS pathway members. Combined with previous studies our findings suggest that separate origins of trait exaggeration among insect lineages were enabled through the independent cooption of IIS, yet via reliance on different components therein

qPCR data

qPCR data for larvae and pupae

Horn measurements-all treatments

Measurements for horn size- body size allometries for all treatments

Data from: Evidence of developmental niche construction in dung beetles: effects on growth, scaling and reproductive success

Niche construction occurs when organisms modify their environments and alter selective conditions through their physiology and behaviours. Such modifications can bias phenotypic variation and enhance organism–environment fit. Yet few studies exist that experimentally assess the degree to which environmental modifications shape developmental and fitness outcomes, how their influences may differ among species and identify the underlying proximate mechanisms. Here, we experimentally eliminate environmental modifications from the developmental environment of Onthophagus dung beetles. We show that these modifications (1) differentially influence growth among species, (2) consistently shape scaling relationships in fitness-related traits, (3) are necessary for the maintenance of sexual dimorphism, (4) influence reproductive success among females of at least one species and (5) implicate larval cultivation of an external rumen as a possible mechanism for environmental modification. Our results present evidence that Onthophagus larvae engage in niche construction, and that this is a fundamental component of beetle development and fitness

Nutrition-responsive gene expression and the developmental evolution of insect polyphenism

Nutrition-responsive development is a ubiquitous and highly diversified example of phenotypic plasticity, yet its underlying molecular and developmental mechanisms and modes of evolutionary diversification remain poorly understood. We measured genome-wide transcription in three closely related species of horned beetles exhibiting strikingly diverse degrees of nutrition responsiveness in the development of male weaponry. We show that (1) counts of differentially expressed genes between low- and high-nutritional backgrounds mirror species-specific degrees of morphological nutrition responsiveness; (2) evolutionary exaggeration of morphological responsiveness is underlain by both amplification of ancestral nutrition-responsive gene expression and recruitment of formerly low nutritionally responsive genes; and (3) secondary loss of morphological responsiveness to nutrition coincides with a dramatic reduction in gene expression plasticity. Our results further implicate genetic accommodation of ancestrally high variability of gene expression plasticity in both exaggeration and loss of nutritional plasticity, yet reject a major role of taxon-restricted genes in the developmental regulation and evolution of nutritional plasticity.Fil: Casasa, Sofia. Indiana University; Estados UnidosFil: Zattara, Eduardo Enrique. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; ArgentinaFil: Moczek, Armin P.. Indiana University; Estados Unido

Assessing the evolutionary lability of insulin signalling in the regulation of nutritional plasticity across traits and species of horned dung beetles

Nutrition-dependent growth of sexual traits is a major contributor to phenotypic diversity, and a large body of research documents insulin signalling as a major regulator of nutritional plasticity. However, findings across studies raise the possibility that the role of individual components within the insulin signalling pathway diverges in function among traits and taxa. Here, we use RNAi-mediated transcript depletion in the gazelle dung beetle to investigate the functions of forkhead box O (Foxo) and two paralogs of the insulin receptor (InR1 and InR2) in shaping nutritional plasticity in polyphenic male head horns, exaggerated fore legs, and weakly nutrition-responsive genitalia. Our functional genetic manipulations led to three main findings: FoxoRNAi reduced the length of exaggerated head horns in large males, while neither InR1 nor InR2 knock-downs resulted in measurable horn phenotypes. These results are similar to those documented previously for another dung beetle (Onthophagus taurus), but in stark contrast to findings in rhinoceros beetles. Secondly, knockdown of Foxo, InR1, and InR2 led to an increase in the intercept or slope of the scaling relationship of genitalia size. These findings are in contrast even to results documented previously for O. taurus. Lastly, while FoxoRNAi reduces male forelegs in D. gazella and O. taurus, the effects of InR1 and InR2 knockdowns diverged across dung beetle species. Our results add to the growing body of literature indicating that despite insulin signalling's conserved role as a regulator of nutritional plasticity, the functions of its components may diversify among traits and species, potentially fuelling the evolution of scaling relationships