scholarly journals A release from developmental bias accelerates morphological diversification in butterfly eyespots

Author(s):  
Oskar Brattström ◽  
Kwaku Aduse-Poku ◽  
Erik van Bergen ◽  
Vernon French ◽  
Paul M. Brakefield

AbstractDevelopment can bias the independent evolution of traits sharing ontogenetic pathways, making certain evolutionary changes less likely. The eyespots commonly found on butterfly wings each have concentric rings of differing colors and these serially repeated pattern elements have been a focus for evo-devo research. In the butterfly family Nymphalidae, eyespots have been shown to function in startling or deflecting predators, and to be involved in sexual selection. Previous work on a model species of Mycalesina butterfly, Bicyclus anynana, has provided insights into the developmental control of the size and color composition of individual eyespots. Experimental evolution has also shown that the relative size of a pair of eyespots on the same wing surface is highly flexible, whereas they are resistant to diverging in color-composition, presumably due to the underlying shared developmental process. This fixed color-composition has been considered as a prime example of developmental bias with significant consequences for wing pattern evolution. Here we test this proposal by surveying eyespots across the whole subtribe of Mycalesina butterflies and demonstrate that developmental bias shapes evolutionary diversification, except in the genus Heteropsis which has gained independent control of eyespot color-composition. Experimental manipulations of pupal wings reveal that the bias has been released through a novel regional response of the wing tissue to a conserved patterning signal. Our study demonstrates that development can bias the evolutionary independence of traits, but it also shows how bias can be released through developmental innovations, thus allowing rapid morphological change, facilitating evolutionary diversification.

2020 ◽  
Vol 117 (44) ◽  
pp. 27474-27480 ◽  
Author(s):  
Oskar Brattström ◽  
Kwaku Aduse-Poku ◽  
Erik van Bergen ◽  
Vernon French ◽  
Paul M. Brakefield

Development can bias the independent evolution of traits sharing ontogenetic pathways, making certain evolutionary changes less likely. The eyespots commonly found on butterfly wings each have concentric rings of differing colors, and these serially repeated pattern elements have been a focus for evo–devo research. In the butterfly family Nymphalidae, eyespots have been shown to function in startling or deflecting predators and to be involved in sexual selection. Previous work on a model species of Mycalesina butterfly,Bicyclus anynana, has provided insights into the developmental control of the size and color composition of individual eyespots. Experimental evolution has also shown that the relative size of a pair of eyespots on the same wing surface is highly flexible, whereas they are resistant to diverging in color composition, presumably due to the underlying shared developmental process. This fixed color composition has been considered as a prime example of developmental bias with significant consequences for wing pattern evolution. Here, we test this proposal by surveying eyespots across the whole subtribe of Mycalesina butterflies and demonstrate that developmental bias shapes evolutionary diversification except in the genusHeteropsiswhich has gained independent control of eyespot color composition. Experimental manipulations of pupal wings reveal that the bias has been released through a novel regional response of the wing tissue to a conserved patterning signal. Our study demonstrates that development can bias the evolutionary independence of traits, but it also shows how bias can be released through developmental innovations, thus, allowing rapid morphological change, facilitating evolutionary diversification.


2011 ◽  
Vol 366 (1574) ◽  
pp. 2069-2075 ◽  
Author(s):  
Paul M. Brakefield

Evo-devo has led to dramatic advances in our understanding of how the processes of development can contribute to explaining patterns of evolutionary diversification that underlie the endless forms of animal life on the Earth. This is increasingly the case not only for the origins of evolutionary novelties that permit new functions and open up new adaptive zones, but also for the processes of evolutionary tinkering that occur within the subsequent radiations of related species. Evo-devo has time and again yielded spectacular examples of Darwin's notions of common ancestry and of descent with modification. It has also shown that the evolution of endless forms is more about the evolution of the regulatory machinery of ancient genes than the origin and elaboration of new genes. Evolvability, especially with respect to the capacity of a developmental system to evolve and to generate the variation in form for natural selection to screen, has become a pivotal focus of evo-devo. As a consequence, a balancing of the concept of endless forms in morphospace with a greater awareness of the potential for developmental constraints and bias is becoming more general. The prospect of parallel horizons opening up for the evolution of behaviour is exciting; in particular, does Sean Carroll's phrase referring to old genes learning new tricks in the evolution of endless forms apply equally as well to patterns of diversity and disparity in behavioural trait-space?


2019 ◽  
Author(s):  
Ian W. Keesey ◽  
Jin Zhang ◽  
Ana Depetris-Chauvin ◽  
George F. Obiero ◽  
Markus Knaden ◽  
...  

Comparative analysis of multiple genomes has been used extensively to examine the evolution of chemosensory receptors across the genus Drosophila. However, few studies have delved into functional characteristics, as most have relied exclusively on genomic data alone, especially for non-model species. In order to increase our understanding of olfactory evolution, we have generated a comprehensive assessment of the olfactory functions associated with the antenna and palps for Drosophila suzukii as well as several other members of the subgenus Sophophora, thus creating a functional olfactory landscape across a total of 20 species. Here we identify and describe several common elements of evolution, including consistent changes in ligand spectra as well as relative receptor abundance, which appear heavily correlated with the known phylogeny. We also combine our functional ligand data with protein orthologue alignments to provide a high-throughput evolutionary assessment and predictive model, where we begin to examine the underlying mechanisms of evolutionary changes utilizing both genetics and odorant binding affinities. In addition, we document that only a few receptors frequently vary between species, and we evaluate the justifications for evolution to reoccur repeatedly within only this small subset of available olfactory sensory neurons.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Ryan A. York ◽  
Allie Byrne ◽  
Kawther Abdilleh ◽  
Chinar Patil ◽  
Todd Streelman ◽  
...  

AbstractThe evolutionary diversification of animal behavior is often associated with changes in the structure and function of nervous systems. Such evolutionary changes arise either through alterations of individual neural components (“mosaically”) or through scaling of the whole brain (“concertedly”). Here we show that the evolution of a courtship behavior in Malawi cichlid fish is associated with rapid, extensive, and specific diversification of orosensory, gustatory centers in the hindbrain. We find that hindbrain volume varies significantly between species that build pit (depression) compared to castle (mound) type bowers and that this trait is evolving rapidly among castle-building species. Molecular analyses of neural activity via immediate early gene expression indicate a functional role for hindbrain structures during bower building. Finally, comparisons of bower building species in neighboring Lake Tanganyika suggest parallel patterns of neural diversification to those in Lake Malawi. Our results suggest that mosaic brain evolution via alterations to individual brain structures is more extensive and predictable than previously appreciated.


2021 ◽  
Author(s):  
Andrew W. Thompson ◽  
Harrison Wojtas ◽  
Myles Davoll ◽  
Ingo Braasch

The Rio Pearlfish Nematolebias whitei is a bi-annual killifish species inhabiting seasonal pools of the Rio de Janeiro region that dry twice per year. Embryos enter dormant diapause stages in the soil, waiting for the inundation of the habitat which triggers hatching and commencement of a new life cycle. This species represents a convergent, independent origin of annualism from other emerging killifish model species. While some transcriptomic datasets are available for Rio Pearlfish, thus far a sequenced genome has been unavailable. Here we present a high quality, 1.2Gb chromosome-level genome assembly, genome annotations and a comparative genomic investigation of the Rio Pearlfish as representative of a vertebrate clade that evolved environmentally-cued hatching. We show conservation of 3-D genome structure across teleost fish evolution, developmental stages, tissues and cell types. Our analysis of mobile DNA shows that Rio Pearlfish, like other annual killifishes, possesses an expanded transposable element profile with implications for rapid aging and adaptation to harsh conditions. We use the Rio Pearlfish genome to identify its hatching enzyme gene repertoire and the location of the hatching gland, a key first step in understanding the developmental genetic control of hatching. The Rio Pearlfish genome expands the comparative genomic toolkit available to study convergent origins of seasonal life histories, diapause, and rapid aging phenotypes. We present the first set of genomic resources for this emerging model organism, critical for future functional genetic and multi-omic explorations of Eco-Evo-Devo phenotypes in resilience and adaptation to extreme environments.


2021 ◽  
Author(s):  
Yun Hee Chang ◽  
Boris I Sheftel ◽  
Bjarke Jensen

Shrews occupy the lower extreme of the seven orders of magnitude mammals range in size. Their hearts are large relative to body weight and heart rate can exceed a thousand beats a minute. To investigate whether cardiac traits that are typical mammalian scale to these extremes, we assessed the heart of three species of shrew (genus Sorex) following the sequential segmental analysis developed for human hearts. Using micro-computed tomography we describe the overall structure and find, in agreement with previous studies, a large and elongate ventricle. The atrial and ventricular septums and the atrioventricular and arterial valves are typically mammalian. The ventricular walls comprise mostly compact myocardium and especially the right ventricle has few trabeculations on the luminal side. A developmental process of compaction is thought to reduce trabeculations in mammals, but in embryonic shrews the volume of trabeculations increase for every gestational stage, only slower than the compact volume. By expression of Hcn4, we identify a sinus node and an atrioventricular conduction axis which is continuous with the ventricular septal crest. Outstanding traits include pulmonary venous sleeve myocardium that reaches farther into the lungs than in any other mammals. Typical proportions of coronary arteries-to-aorta do not scale and the shrew coronary arteries are proportionally enormous, presumably to avoid the high resistance to blood flow of narrow vessels. In conclusion, most cardiac traits do scale to the miniscule shrews. The shrew heart, nevertheless, stands out by its relative size, elongation, proportionally large coronary vessels, and extent of pulmonary venous myocardium.


2018 ◽  
Author(s):  
Ryan A. York ◽  
Allie Byrne ◽  
Kawther Abdhilleh ◽  
Chinar Patil ◽  
J. Todd Streelman ◽  
...  

AbstractThe evolutionary diversification of animal behavior is often associated with changes in the structure and function of nervous systems. Such evolutionary changes arise either through alterations of individual neural components (“mosaically”) or through scaling of the whole brain (“conceitedly”). Here we show that the evolution of a specific courtship behavior in Malawi cichlid fish, the construction of mating nests known as bowers, is associated with rapid, extensive, and specific diversification of orosensory, gustatory centers in the hindbrain. We find that hindbrain volume varies significantly between species that build pit (depression) compared to castle (mound) type bowers and that hindbrain features evolve rapidly and independently of phylogeny among castle-building species. Using immediate early gene expression, we confirmed a functional role for hindbrain structures during bower building. Comparisons of bower building species in neighboring Lake Tanganyika show patterns of neural diversification parallel to those in Lake Malawi. Our results suggest that mosaic brain evolution via alterations to individual brain structures is more extensive and predictable than previously appreciated.


2017 ◽  
Author(s):  
Fumihiro Ito ◽  
Tomotaka Matsumoto ◽  
Tatsumi Hirata

AbstractMorphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale using the teleost. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony-based methods—event-pairing (Jeffery, Bininda-Emonds, Coates & Richardson, 2002a) and continuous analysis (Germain & Laurin, 2009). The phylogenetic comparisons of these sequences revealed event-dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. The phylogenetic analyses suggested that the ancestral species had experienced frequent changes in developmental sequences. Although the analyses showed that these heterochronic changes accumulated along phylogenic time, the precise distribution of the changes over the teleost phylogeny remains unclear due to technical limitations. Finally, this first comprehensive analysis of teleost developmental sequences will provide solid ground on which to elucidate the significance of developmental timing in animal morphological diversification.


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