scholarly journals Neural divergence and hybrid disruption between ecologically isolated Heliconius butterflies

2021 ◽  
Vol 118 (6) ◽  
pp. e2015102118 ◽  
Author(s):  
Stephen H. Montgomery ◽  
Matteo Rossi ◽  
W. Owen McMillan ◽  
Richard M. Merrill
Keyword(s):  
Gene Expression ◽  
Gene Flow ◽  
Sympatric Species ◽  
Mate Preferences ◽  
Brain Morphology ◽  
Neural Systems ◽  
Close Relatives ◽  
Neuroanatomical Data ◽  
Intermediate Traits ◽  
Heliconius Cydno

The importance of behavioral evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. A handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation. However, the degree to which brains are adapted to local environmental conditions, and whether this contributes to reproductive isolation between close relatives that have diverged in ecology, remains unknown. Here, we examine divergence in brain morphology and neural gene expression between closely related, but ecologically distinct, Heliconius butterflies. Despite ongoing gene flow, sympatric species pairs within the melpomene–cydno complex are consistently separated across a gradient of open to closed forest and decreasing light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that Heliconius melpomene and Heliconius cydno clades have substantial shifts in brain morphology across their geographic range, with divergent structures clustered in the visual system. These neuroanatomical differences are mirrored by extensive divergence in neural gene expression. Differences in both neural morphology and gene expression are heritable, exceed expected rates of neutral divergence, and result in intermediate traits in first-generation hybrid offspring. Strong evidence of divergent selection implies local adaptation to distinct selective optima in each parental microhabitat, suggesting the intermediate traits of hybrids are poorly matched to either condition. Neural traits may therefore contribute to coincident barriers to gene flow, thereby helping to facilitate speciation.

scholarly journals Neural divergence and hybrid disruption between ecologically isolated Heliconius butterflies

2020 ◽  
Author(s):  
Stephen H. Montgomery ◽  
Matteo Rossi ◽  
W. Owen McMillan ◽  
Richard M. Merrill
Keyword(s):  
Gene Expression ◽  
Gene Flow ◽  
Sympatric Species ◽  
Neural System ◽  
Mate Preferences ◽  
Brain Morphology ◽  
Disruptive Selection ◽  
Neural Function ◽  
Environmental Transitions ◽  
Neuroanatomical Data

SummaryThe importance of behavioural evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. Although a handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation, how brains respond to broad environmental transitions, and whether this contributes to reproductive isolation, remains unknown. Here, we examine divergence in brain morphology and neural gene expression between closely related, but ecologically distinct, Heliconius butterflies. Despite on-going gene flow, sympatric species pairs within the melpomene-cydno complex are consistently separated across a gradient of open to closed forest and decreasing light intensity. By generating quantitative neuroanatomical data for 107 butterflies, we show that H. melpomene and H. cydno have substantial shifts in brain morphology across their geographic range, with divergent structures clustered in the visual system. These neuroanatomical differences are mirrored by extensive divergence in neural gene expression. Differences in both morphology and gene expression are heritable, exceed expected rates of neutral divergence, and result in intermediate traits in first generation hybrid offspring. This likely disrupts neural system function, leading to a mismatch between the environment and the behavioral response of hybrids. Our results suggest that disruptive selection on both neural function and external morphology result in coincident barriers to gene flow, thereby facilitating speciation.

scholarly journals Physical Linkage and Mate Preference Generate Linkage Disequilibrium for Behavioral Isolation in two Parapatric Crickets

2018 ◽  
Author(s):  
Thomas Blankers ◽  
Emma L. Berdan ◽  
R. Matthias Hennig ◽  
Frieder Mayer
Keyword(s):  
Gene Expression ◽  
Linkage Disequilibrium ◽  
Gene Flow ◽  
Major Effect ◽  
Mate Preferences ◽  
Genetic Covariance ◽  
Male And Female ◽  
Behavioral Isolation ◽  
Physical Linkage ◽  
Preference Functions

ABSTRACTBehavioral isolation is a potent barrier to gene flow and a source of striking diversity in the animal kingdom. However, it remains unclear if the linkage disequilibrium (LD) between sex-specific traits required for behavioral isolation results mostly from physical linkage between signal and preference loci or from directional mate preferences. Here, we test this in the field crickets Gryllus rubens and G. texensis. These closely related species diverged with gene flow and have strongly diverged songs and preference functions for the mate calling song rhythm. We map quantitative trait loci for signal and preference traits (pQTL) as well as for gene expression associated with these traits (eQTL). We find strong, positive genetic covariance between song traits and between song and preference. Our results show that this is in part explained by incomplete physical linkage: although both linked pQTL and eQTL couple male and female traits, major effect loci for different traits were never on the same chromosome. We suggest that the finely-tuned, highly divergent preference functions are likely an additional source of LD between male and female traits in this system. Furthermore, pleiotropy of gene expression presents an underappreciated mechanism to link sexually dimorphic phenotypes.

scholarly journals Comparative transcriptomics of sympatric species of coral reef fishes (genus: Haemulon)

PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e6541 ◽  
Author(s):  
Moisés A. Bernal ◽  
Groves B. Dixon ◽  
Mikhail V. Matz ◽  
Luiz A. Rocha
Keyword(s):  
Gene Expression ◽  
Immune Response ◽  
Coral Reef ◽  
Positive Selection ◽  
Reef Fishes ◽  
Sympatric Species ◽  
Coral Reef Fishes ◽  
Western Atlantic ◽  
Morphological Studies ◽  
Fish Samples

Background Coral reefs are major hotspots of diversity for marine fishes, yet there is still ongoing debate on the mechanisms that promote divergence in these rich ecosystems. Our understanding of how diversity originates in this environment could be enhanced by investigating the evolutionary dynamics of closely related fishes with overlapping ranges. Here, we focus on grunts of the genus Haemulon, a group of coral reef fishes with 15 species in the Western Atlantic, 11 of which are syntopic. Methods Wild fish samples from three sympatric species of the Caribbean: Haemulon flavolineatum, H. carbonarium and H. macrostomum, were collected while SCUBA diving. RNA was extracted from livers, and the transcriptomes were assembled and annotated to investigate positive selection (Pairwise dN/dS) and patterns of gene expression between the three species. Results Pairwise dN/dS analyses showed evidence of positive selection for genes associated with immune response, cranial morphology and formation of the anterior–posterior axis. Analyses of gene expression revealed that despite their sympatric distribution, H. macrostomum showed upregulation of oxidation-reduction machinery, while there was evidence for activation of immune response in H. carbonarium. Discussion Overall, our analyses suggest closely related grunts show important differences in genes associated with body shape and feeding morphology, a result in-line with previous morphological studies in the group. Further, despite their overlapping distribution they interact with their environment in distinct fashions. This is the largest compendium of genomic information for grunts thus far, representing a valuable resource for future studies in this unique group of coral reef fishes.

scholarly journals Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

2017 ◽  
Author(s):  
Steven M. Van Belleghem ◽  
Margarita Baquero ◽  
Riccardo Papa ◽  
Camilo Salazar ◽  
W. Owen McMillan ◽  
...  
Keyword(s):  
Gene Flow ◽  
Sex Chromosome ◽  
Null Model ◽  
Sympatric Species ◽  
Ancestral Population ◽  
Z Chromosome ◽  
Butterfly Species ◽  
Species Pairs ◽  
Species Comparisons ◽  
Strong Barrier

AbstractSex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a ‘large-X’ effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, i.e. ‘faster-X’, or barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply post-zygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of species incompatibilities. Our work demonstrates the importance of constructing an appropriate demographic null model in order to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

Do Hind Wing Eyespots of Caligo Butterflies Function in Both Mating Behavior and Antipredator Defense? (Lepidoptera, Nymphalidae)

2020 ◽  
Author(s):  
Logan D Crees ◽  
Phil DeVries ◽  
Carla M Penz
Keyword(s):  
Hind Wing ◽  
Phylogenetic Signal ◽  
Positive Association ◽  
Sympatric Species ◽  
Color Pattern ◽  
Visual Signal ◽  
Antipredator Defense ◽  
Predator Prey ◽  
Close Relatives ◽  
Relationship Of

Abstract In general, butterfly ventral hind wing eyespots are considered to play a role in predator–prey interactions. These eyespots are prominent wing pattern elements in Brassolini butterflies, and they vary in size, position, and number across taxa. Female Caligo Hübner, 1819 (Lepidoptera, Nymphalidae) appear to use the large eyespots of lekking males as a mate-locating cue, but female Opsiphanes Doubleday, 1849 (Lepidoptera, Nymphalidae) do not because males patrol to find mates. These behaviors led us to predict that male Caligo should have larger eyespots than females, but eyespot size would not differ between sexes in Opsiphanes. Our analyses supported these predictions. As displacement of the eyespots to the center of the wing might make them more conspicuous, we asked if eyespot position and size covaried across the Brassolini phylogeny. While we found a positive association between position and size, the relationship of these two variables contained significant phylogenetic signal. Two Brassolini species show strong sexual dimorphism where females converge on the color pattern of sympatric species of Caligo. Their ventral hind wing eyespots are much larger than those of close relatives, approximating those of Caligo, and further reinforcing the importance of ventral hind wing eyespots as a visual signal in this group of butterflies. Importantly, our results suggest that, in addition to antipredation defense, ventral hind wing eyespots can function in mating activities, and consequently they might be evolving under both natural and sexual selection in Caligo butterflies.

scholarly journals Landscape, colonization, and life history: their effects on genetic diversity in four sympatric species inhabiting a dendritic system

2019 ◽  
Vol 76 (12) ◽  
pp. 2288-2302 ◽  
Author(s):  
Daniel E. Ruzzante ◽  
Gregory R. McCracken ◽  
Sarah J. Salisbury ◽  
Hilary T. Brewis ◽  
Donald Keefe ◽  
...  
Keyword(s):  
Genetic Diversity ◽  
Gene Flow ◽  
Lake Trout ◽  
Sympatric Species ◽  
Genetic Structuring ◽  
Colonization History ◽  
Diversity Patterns ◽  
Contemporary Gene Flow ◽  
Approximate Bayesian ◽  
Longnose Sucker

To what degree are patterns of genetic structure in fragmented systems the result of contemporary landscape versus history? We examined the distribution of genetic diversity as a function of colonization history and contemporary landscape in four fish species inhabiting a hierarchically fragmented, unaltered system, the Kogaluk drainage (Labrador): lake trout (Salvelinus namaycush), longnose sucker (Catostomus catostomus), round whitefish (Prosopium cylindraceum), and lake chub (Couesius plumbeus). The footprint of colonization history was still observable in the three species where this issue was examined regardless of the generations since their arrival. Approximate Bayesian computation (ABC) analyses suggest colonization took place from the southwest. The species exhibit similar diversity patterns despite different [Formula: see text] values and generation intervals. Contemporary gene flow was largely negligible except for gene flow from a centrally located lake. These results suggest landscape has driven colonization history, which still has influence on genetic structuring. The species are widespread. Understanding how they behave in the pristine Kogaluk provides a baseline against which to evaluate how other anthropogenically perturbed systems are performing. Improved understanding of historical and contemporary processes is required to fully explain diversity patterns in complex metapopulations.

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