Evolution in similar environments often leads to convergence of behavioral and anatomical traits. A classic example of convergent trait evolution is the reduced traits that characterize many cave animals: reduction or loss of pigmentation and eyes. While these traits have evolved many times, relatively little is known about whether these traits repeatedly evolve through the same or different molecular and developmental mechanisms. The small freshwater fish,
- Award ID(s):
- 1759906
- NSF-PAR ID:
- 10190679
- Date Published:
- Journal Name:
- Genes
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2073-4425
- Page Range / eLocation ID:
- 42
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Astyanax mexicanus , provides an opportunity to investigate the repeated evolution of cave traits.A. mexicanus exists as two forms, a sighted, surface‐dwelling form and at least 29 populations of a blind, cave‐dwelling form that initially develops eyes that subsequently degenerate. We compared eye morphology and the expression of eye regulatory genes in developing surface fish and two independently evolved cavefish populations, Pachón and Molino. We found that many of the previously described molecular and morphological alterations that occur during eye development in Pachón cavefish are also found in Molino cavefish. However, for many of these traits, the Molino cavefish have a less severe phenotype than Pachón cavefish. Further, cave–cave hybrid fish have larger eyes and lenses during early development compared with fish from either parental population, suggesting that some different changes underlie eye loss in these two populations. Together, these data support the hypothesis that these two cavefish populations evolved eye loss independently, yet through some of the same developmental and molecular mechanisms. -
null (Ed.)Abstract Background Arachnids are important components of cave ecosystems and display many examples of troglomorphisms, such as blindness, depigmentation, and elongate appendages. Little is known about how the eyes of arachnids are specified genetically, let alone the mechanisms for eye reduction and loss in troglomorphic arachnids. Additionally, duplication of Retinal Determination Gene Network (RDGN) homologs in spiders has convoluted functional inferences extrapolated from single-copy homologs in pancrustacean models. Results We investigated a sister species pair of Israeli cave whip spiders, Charinus ioanniticus and C. israelensis (Arachnopulmonata, Amblypygi), of which one species has reduced eyes. We generated embryonic transcriptomes for both Amblypygi species, and discovered that several RDGN homologs exhibit duplications. We show that duplication of RDGN homologs is systemic across arachnopulmonates (arachnid orders that bear book lungs), rather than being a spider-specific phenomenon. A differential gene expression (DGE) analysis comparing the expression of RDGN genes in field-collected embryos of both species identified candidate RDGN genes involved in the formation and reduction of eyes in whip spiders. To ground bioinformatic inference of expression patterns with functional experiments, we interrogated the function of three candidate RDGN genes identified from DGE using RNAi in the spider Parasteatoda tepidariorum . We provide functional evidence that one of these paralogs, sine oculis/Six1 A ( soA ), is necessary for the development of all arachnid eye types. Conclusions Our work establishes a foundation to investigate the genetics of troglomorphic adaptations in cave arachnids, and links differential gene expression to an arthropod eye phenotype for the first time outside of Pancrustacea. Our results support the conservation of at least one RDGN component across Arthropoda and provide a framework for identifying the role of gene duplications in generating arachnid eye diversity.more » « less
-
more » « less
Abstract Extreme environments often result in the evolution of dramatic adaptive features. The Mexican tetra,
Astyanax mexicanus , includes 30 different populations of cave‐dwelling forms that live in perpetual darkness. As a consequence, many populations have evolved eye loss, reduced pigmentation, and amplification of nonvisual sensory systems. Closely‐related surface‐dwelling morphs demonstrate typical vision, pigmentation, and sensation. Transcriptomic assessments in this system have revealed important developmental changes associated with the cave morph, however, they have not accounted for photic rearing conditions. Prior studies reared individuals under a 12:12 hr light/dark (LD) cycle. Here, we reared cavefish under constant darkness (DD) for 5+ years. From these experimental individuals, we performed mRNA sequencing and compared gene expression of surface fish reared under LD conditions to cavefish reared under DD conditions to identify photic‐dependent gene expression differences. Gene Ontology enrichment analyses revealed a number of previously underappreciated cave‐associated changes impacting blood physiology and olfaction. We further evaluated the position of differentially expressed genes relative to QTL positions from prior studies and found several candidate genes associated with these ecologically relevant lighting conditions. In sum, this work highlights photic conditions as a key environmental factor impacting gene expression patterns in blind cave‐dwelling fish. -
more » « less
Throughout the evolutionary tree, there are gains and losses of morphological features, physiological processes, and behavioral patterns. Losses are perhaps nowhere so prominent as for subterranean organisms, which typically show reductions or losses of eyes and pigment. These losses seem easy to explain without recourse to natural selection. Its most modern form is the accumulation of selectively neutral, structurally reducing mutations. Selectionist explanations include direct selection, often involving metabolic efficiency in resource poor subterranean environments, and pleiotropy, where genes affecting eyes and pigment have other effects, such as increasing extra-optic sensory structures. This dichotomy echoes the debate in evolutionary biology in general about the sufficiency of natural selection as an explanation of evolution, e.g., Kimura’s neutral mutation theory. Tests of the two hypotheses have largely been one-sided, with data supporting that one or the other processes is occurring. While these tests have utilized a variety of subterranean organisms, the Mexican cavefish,
Astyanax mexicanus , which has eyed extant ancestral-like surface fish conspecifics, is easily bred in the lab, and whose whole genome has been sequenced, is the favored experimental organism. However, with few exceptions, tests for selection versus neutral mutations contain limitations or flaws. Notably, these tests are often one sided, testing for the presence of one or the other process. In fact, it is most likely that both processes occur and make a significant contribution to the two most studied traits in cave evolution: eye and pigment reduction. Furthermore, narrow focus on neutral mutation hypothesis versus selection to explain cave-evolved traits often fails, at least in the simplest forms of these hypotheses, to account for aspects that are likely essential for understanding cave evolution: migration or epigenetic effects. Further, epigenetic effects and phenotypic plasticity have been demonstrated to play an important role in cave evolution in recent studies. Phenotypic plasticity does not by itself result in genetic change of course, but plasticity can reveal cryptic genetic variation which then selection can act on. These processes may result in a radical change in our thinking about evolution of subterranean life, especially the speed with which it may occur. Thus, perhaps it is better to ask what role the interaction of genes and environment plays, in addition to natural selection and neutral mutation. -
Abstract Butterfly eyes are complex organs that are composed of a diversity of proteins and they play a central role in visual signaling and ultimately, speciation, and adaptation. Here, we utilized the whole eye transcriptome to obtain a more holistic view of the evolution of the butterfly eye while accounting for speciation events that co-occur with ancient hybridization. We sequenced and assembled transcriptomes from adult female eyes of eight species representing all major clades of the Heliconius genus and an additional outgroup species, Dryas iulia. We identified 4,042 orthologous genes shared across all transcriptome data sets and constructed a transcriptome-wide phylogeny, which revealed topological discordance with the mitochondrial phylogenetic tree in the Heliconius pupal mating clade. We then estimated introgression among lineages using additional genome data and found evidence for ancient hybridization leading to the common ancestor of Heliconius hortense and Heliconius clysonymus. We estimated the Ka/Ks ratio for each orthologous cluster and performed further tests to demonstrate genes showing evidence of adaptive protein evolution. Furthermore, we characterized patterns of expression for a subset of these positively selected orthologs using qRT-PCR. Taken together, we identified candidate eye genes that show signatures of adaptive molecular evolution and provide evidence of their expression divergence between species, tissues, and sexes. Our results demonstrate: 1) greater evolutionary changes in younger Heliconius lineages, that is, more positively selected genes in the cydno–melpomene–hecale group as opposed to the sara–hortense–erato group, and 2) suggest an ancient hybridization leading to speciation among Heliconius pupal-mating species.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.3390/genes11010042
