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Background Natural model systems are indispensable for exploring adaptations in response to environmental pressures.Sinocyclocheilusof China, the most diverse cavefish clade in the world (75 species), provide unique opportunities to understand recurrent evolution of stereotypic traits (such as eye loss and sensory expansion) in the context of a deep and diverse phylogenetic group. However, they remain poorly understood in terms of their morphological evolution. Therefore, we explore key patterns of morphological evolution, habitat utilization and geographic distribution in these fishes. Results We constructed phylogenies and categorized 49 species based on eye-related condition (Blind, Micro-eyed, and Normal-eyed), habitat types (Troglobitic—cave-restricted; Troglophilic—cave-associated; Surface—outside caves) and existence of horns. Geometric-morphometric analyses show Normal-eyed morphs with fusiform shapes segregating from Blind/Micro-eyed deeper bodied morphs along the first principal-component axis; second axis accounts for shape complexity related to horns. The body shapes showed a significant association with eye-related condition and horn, but not habitat types. Ancestral reconstructions suggest at least three independent origins of Blind morphs, each with different levels of modification in relation to their ancestral Normal-eyed morphs;Sinocyclocheilusare also pre-adapted for cave dwelling. Our geophylogeny shows an east-to-west diversification spanning Pliocene and Pleistocene, with early-diversifying Troglobitic species dominating subterranean habitats of karstic plains whereas predominantly Surface forms inhabit hills to the west. Evolutionary rates analyses suggest that lineages leading to Blind morphs were characterized by significant rate shifts, such as a slowdown in body size evolution and a 5–20 fold increase in rate of eye regression, possibly explained by limited resource availability. Body size and eye size have undergone reversals, but not horns, a trait entailing considerable time to form. Conclusions Sinocyclocheilusoccupied cave habitats in response to drying associated with aridification of China during late Miocene and the Pliocene. The prominent cave-adaptations (eye-regression, horn-evolution) occur in clades associated with the extensive subterranean cave system in Guangxi and Guizhou provinces. Integration of morphology, phylogeny, rate analyses, molecular-dating and distribution show not only several remarkable patterns of evolution, but also interesting exceptions to these patterns signifying the diversification ofSinocyclocheilusas an invaluable model system to explore evolutionary novelty.
Ting-Ru Mao; Ye-Wei Liu; Madhava Meegaskumbura; Jian Yang; Gajaba Ellepola; Gayani Senevirathne; Cheng-Hai Fu; Joshua B. Gross; Marcio R. Pie. Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals, and origin of novel traits. BMC Ecology and Evolution 2021, 21, 1 -14.
AMA StyleTing-Ru Mao, Ye-Wei Liu, Madhava Meegaskumbura, Jian Yang, Gajaba Ellepola, Gayani Senevirathne, Cheng-Hai Fu, Joshua B. Gross, Marcio R. Pie. Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals, and origin of novel traits. BMC Ecology and Evolution. 2021; 21 (1):1-14.
Chicago/Turabian StyleTing-Ru Mao; Ye-Wei Liu; Madhava Meegaskumbura; Jian Yang; Gajaba Ellepola; Gayani Senevirathne; Cheng-Hai Fu; Joshua B. Gross; Marcio R. Pie. 2021. "Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals, and origin of novel traits." BMC Ecology and Evolution 21, no. 1: 1-14.
Extreme environmental features can drive the evolution of extreme phenotypes. Over the course of evolution, certain environmental changes may be so drastic that they lead to extinction. Conversely, if an organism adapts to harsh environmental changes, the adaptations may permit expansion of a novel niche. The interaction between environmental stressors and adaptive changes is well-illustrated by the blind Mexican cavefish, Astyanaxmexicanus, which has recurrently adapted to the stark subterranean environment. The transition from terrestrial rivers and streams (occupied by extant surface morphs of the same species) to the cave has been accompanied by the resorption of eyes, diminished pigmentation and reduced metabolism in cave-dwelling morphs. The principal features of caves most often associated with evolution of these common cave features are the absence of light and limited nutrition. However, a putatively essential cave feature that has received less attention is the frequently low concentration of oxygen within natural karst environments. Here, we review the potential role of limited oxygen as a critical environmental feature of caves in the Sierra de El Abra. Additionally, we review evidence that Astyanax cavefish may have evolved adaptive features enabling them to thrive in lower oxygen compared to their surface-dwelling counterparts.
Tyler Boggs; Joshua Gross. Reduced Oxygen as an Environmental Pressure in the Evolution of the Blind Mexican Cavefish. Diversity 2021, 13, 26 .
AMA StyleTyler Boggs, Joshua Gross. Reduced Oxygen as an Environmental Pressure in the Evolution of the Blind Mexican Cavefish. Diversity. 2021; 13 (1):26.
Chicago/Turabian StyleTyler Boggs; Joshua Gross. 2021. "Reduced Oxygen as an Environmental Pressure in the Evolution of the Blind Mexican Cavefish." Diversity 13, no. 1: 26.
A key challenge in contemporary biology is connecting genotypic variation to phenotypic diversity. Quantitative genetics provides a powerful technique for identifying regions of the genome that covary with phenotypic variation. Here, we present a quantitative trait loci (QTL) analysis of a natural freshwater fish system, Astyanax mexicanus, that harbors two morphs corresponding to a cave and surface fish. Following their divergence ~500 Kya, cavefish have adapted to the extreme pressures of the subterranean biome. As a consequence, cavefish have lost numerous features, but evolved gains for a variety of constructive features including behavior. Prior work found that sensory tissues (neuromasts) present in the “eye orbit” region of the skull associate with sensitivity to vibrations in water. This augmented sensation is believed to facilitate foraging behavior in the complete darkness of a cave, and may impact on evolved lateral swimming preference. To this point, however, it has remained unclear how morphological variation integrates with behavioral variation through heritable factors. Using a QTL approach, we discovered the genetic architecture of neuromasts present in the eye orbit region, demonstrating that this feature is under genetic control. Interestingly, linked loci were asymmetric–signals were detected using only data collected from the right, but not left, side of the face. This finding may explain enhanced sensitivity and/or feedback of water movements mediating a lateral swimming preference. The locus we discovered based on neuromast position maps near established QTL for eye size and a facial bone morphology, raising the intriguing possibility that eye loss, sensory expansion, and the cranial skeleton may be integrated for evolving adaptive behaviors. Thus, this work will further our understanding of the functional consequence of key loci that influence the evolutionary origin of changes impacting morphology, behavior, and adaptation.
Amanda Powers; Tyler Boggs; Joshua Gross. An Asymmetric Genetic Signal Associated with Mechanosensory Expansion in Cave-Adapted Fish. Symmetry 2020, 12, 1951 .
AMA StyleAmanda Powers, Tyler Boggs, Joshua Gross. An Asymmetric Genetic Signal Associated with Mechanosensory Expansion in Cave-Adapted Fish. Symmetry. 2020; 12 (12):1951.
Chicago/Turabian StyleAmanda Powers; Tyler Boggs; Joshua Gross. 2020. "An Asymmetric Genetic Signal Associated with Mechanosensory Expansion in Cave-Adapted Fish." Symmetry 12, no. 12: 1951.
The cover image is based on the Research Article Parallel evolution of regressive and constructive craniofacial traits across distinct populations of Astyanax mexicanus cavefish by Amanda K. Powers et al., https://doi.org/10.1002/jez.b.22932.
Amanda K. Powers; Daniel J. Berning; Joshua B. Gross. Cover Image. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2020, 334, 1 .
AMA StyleAmanda K. Powers, Daniel J. Berning, Joshua B. Gross. Cover Image. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 2020; 334 (7-8):1.
Chicago/Turabian StyleAmanda K. Powers; Daniel J. Berning; Joshua B. Gross. 2020. "Cover Image." Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 334, no. 7-8: 1.
Suzanne E. McGaugh; Johanna E. Kowalko; Erik Duboué; Peter Lewis; Tamara A. Franz‐Odendaal; Nicolas Rohner; Joshua B. Gross; Alex C. Keene. Dark world rises: The emergence of cavefish as a model for the study of evolution, development, behavior, and disease. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2020, 334, 397 -404.
AMA StyleSuzanne E. McGaugh, Johanna E. Kowalko, Erik Duboué, Peter Lewis, Tamara A. Franz‐Odendaal, Nicolas Rohner, Joshua B. Gross, Alex C. Keene. Dark world rises: The emergence of cavefish as a model for the study of evolution, development, behavior, and disease. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 2020; 334 (7-8):397-404.
Chicago/Turabian StyleSuzanne E. McGaugh; Johanna E. Kowalko; Erik Duboué; Peter Lewis; Tamara A. Franz‐Odendaal; Nicolas Rohner; Joshua B. Gross; Alex C. Keene. 2020. "Dark world rises: The emergence of cavefish as a model for the study of evolution, development, behavior, and disease." Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 334, no. 7-8: 397-404.
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.
Connor R. Sears; Tyler E. Boggs; Joshua B. Gross. Dark‐rearing uncovers novel gene expression patterns in an obligate cave‐dwelling fish. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2020, 334, 518 -529.
AMA StyleConnor R. Sears, Tyler E. Boggs, Joshua B. Gross. Dark‐rearing uncovers novel gene expression patterns in an obligate cave‐dwelling fish. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 2020; 334 (7-8):518-529.
Chicago/Turabian StyleConnor R. Sears; Tyler E. Boggs; Joshua B. Gross. 2020. "Dark‐rearing uncovers novel gene expression patterns in an obligate cave‐dwelling fish." Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 334, no. 7-8: 518-529.
Epitomized by the well-studied Astyanax mexicanus, cavefishes provide important model organisms to understand adaptations in response to divergent natural selection. However, the spectacular Sinocyclocheilus diversification of China, the most diverse cavefish clade in the world harboring nearly 75 species, demonstrate evolutionary convergence for many traits, yet remain poorly understood in terms of their morphological evolution. Here, using a broad sample of 49 species representative of this diversification, we analyze patterns of Sinocylocheilus evolution in a phylogenetic context. We categorized species into morphs based on eye-related condition: Blind, Micro-eyed (small-eyed), and Normal-eyed and we also considered three habitat types (Troglodytic – cave-restricted; Troglophilic – cave-associated; Surface – outside of caves). Geometric morphometric analyses show Normal-eyed morphs with fusiform shapes being segregated from Blind/Micro-eyed (Eye-regressed) morphs with deeper bodies along the first principal component (“PC”) axis. The second PC axis accounts for shape complexity related to the presence of horns. Ancestral character reconstructions of morphs suggest at least three independent origins of Blind morphs, each with different levels of modification in relation to the typical morphology of ancestral Normal-eyed morphs. Interestingly, only some Blind or Micro-eyed morphs bear horns and they are restricted to a single clade (Clade B) and arising from a Troglodytic ancestral species. Our geophylogeny shows an east-to-west diversification spanning the Pliocene and the Pleistocene, with Troglodytic species dominating karstic subterranean habitats of the plains whereas predominantly Surface species inhabit streams and pools in hills to the west (perhaps due to the scarcity of caves). Integration of morphology, phylogeny and geography suggests Sinocyclocheilus are pre-adapted for cave dwelling. Analyses of evolutionary rates suggest that lineages leading to Blind morphs were characterized by significant rate shifts, such as a slowdown in body size evolution and a 3.3 to 12.5 fold increase in the evolutionary rate of eye regression. Furthermore, body size and eye size have undergone reversals, but horns have not, a trait that seem to require substantial evolutionary time to form. These results, compared to the Astyanax model system, indicate Sinocyclocheilus fishes demonstrate extraordinary morphological diversity and variation, offering an invaluable model system to explore evolutionary novelty.
Ting-Ru Mao; Ye-Wei Liu; Madhava Meegaskumbura; Jian Yang; Gajaba Ellepola; Gayani Senevirathne; Cheng-Hai Fu; Joshua B. Gross; Marcio R. Pie. Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits. 2020, 1 .
AMA StyleTing-Ru Mao, Ye-Wei Liu, Madhava Meegaskumbura, Jian Yang, Gajaba Ellepola, Gayani Senevirathne, Cheng-Hai Fu, Joshua B. Gross, Marcio R. Pie. Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits. . 2020; ():1.
Chicago/Turabian StyleTing-Ru Mao; Ye-Wei Liu; Madhava Meegaskumbura; Jian Yang; Gajaba Ellepola; Gayani Senevirathne; Cheng-Hai Fu; Joshua B. Gross; Marcio R. Pie. 2020. "Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals and origin of novel traits." , no. : 1.
Life in complete darkness has driven the evolution of a suite of troglobitic features in the blind Mexican cavefish Astyanax mexicanus, such as eye and pigmentation loss. While regressive evolution is a hallmark of obligate cave‐dwelling organisms, constructive (or augmented) traits commonly arise as well. The cavefish cranium has undergone extensive changes compared with closely‐related surface fish. These alterations are rooted in both cranial bones and surrounding sensory tissues such as enhancements in the gustatory and lateral line systems. Cavefish also harbor numerous cranial bone asymmetries: fluctuating asymmetry of individual bones and directional asymmetry in a dorsal bend of the skull. This asymmetry is mirrored by the asymmetrical patterning of mechanosensory neuromasts. We explored the relationship between facial bones and neuromasts using in vivo fluorescent colabeling and microcomputed tomography. We found an increase in neuromast density within dermal bone boundaries across three distinct populations of cavefish compared to surface‐dwelling fish. We also show that eye loss disrupts early neuromast patterning, which in turn impacts the development of dermal bones. While cavefish exhibit alterations in cranial bone and neuromast patterning, each population varied in the severity. This variation may reflect observed differences in behavior across populations. For instance, a bend in the dorsal region of the skull may expose neuromasts to water flow on the opposite side of the face, enhancing sensory input and spatial mapping in the dark.
Amanda K. Powers; Daniel J. Berning; Joshua B. Gross. Parallel evolution of regressive and constructive craniofacial traits across distinct populations of Astyanax mexicanus cavefish. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2020, 334, 450 -462.
AMA StyleAmanda K. Powers, Daniel J. Berning, Joshua B. Gross. Parallel evolution of regressive and constructive craniofacial traits across distinct populations of Astyanax mexicanus cavefish. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. 2020; 334 (7-8):450-462.
Chicago/Turabian StyleAmanda K. Powers; Daniel J. Berning; Joshua B. Gross. 2020. "Parallel evolution of regressive and constructive craniofacial traits across distinct populations of Astyanax mexicanus cavefish." Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 334, no. 7-8: 450-462.
Together, the complex geological history and climatic diversity of Mesoamerica create a rich source of biodiversity from which evolutionary processes can be studied. Here, we discuss highly divergent morphs of lake‐dwelling fishes distributed across Mexico and Central America, originally recognized as members of different genera (Astyanax and “Bramocharax”). Recent phylogenetic studies, however, suggest these morphs group within the same genus and readily hybridize. Despite genetic similarities, Bramocharax morphs exhibit stark differences in cranial shape and dentition. We investigated the evolution of several cranial traits that vary across morphs collected from four lakes in Mexico and Nicaragua and discovered an ecomorphological cline from northern to southern lakes. Northern populations of sympatric morphs exhibit a similar cranial shape and tooth morphology. Southern populations of Bramocharax morphs, however, showed a larger disparity in maxillary teeth, length and frequency of unicuspid teeth, an elongated snout, and a streamlined cranium compared to Astyanax morphs. This divergence of craniofacial morphology likely evolved in association with differences in trophic niches. We discuss the morphological differences across the four lake systems in terms of geological history and trophic dynamics. In summary, our study suggests that Bramocharax morphs are likely locally adapted members derived from independent Astyanax lineages, highlighting an interesting parallel evolutionary pattern within the Astyanax genus.
Amanda K. Powers; Carlos A. Garita‐Alvarado; Rocío Rodiles‐Hernández; Daniel J. Berning; Joshua B. Gross; C. Patricia Ornelas‐García. A geographical cline in craniofacial morphology across populations of Mesoamerican lake‐dwelling fishes. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 2020, 333, 171 -180.
AMA StyleAmanda K. Powers, Carlos A. Garita‐Alvarado, Rocío Rodiles‐Hernández, Daniel J. Berning, Joshua B. Gross, C. Patricia Ornelas‐García. A geographical cline in craniofacial morphology across populations of Mesoamerican lake‐dwelling fishes. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology. 2020; 333 (3):171-180.
Chicago/Turabian StyleAmanda K. Powers; Carlos A. Garita‐Alvarado; Rocío Rodiles‐Hernández; Daniel J. Berning; Joshua B. Gross; C. Patricia Ornelas‐García. 2020. "A geographical cline in craniofacial morphology across populations of Mesoamerican lake‐dwelling fishes." Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 333, no. 3: 171-180.
Cave animals are a fascinating group of species often demonstrating characteristics including reduced eyes and pigmentation, metabolic efficiency, and enhanced sensory systems. Asellus aquaticus, an isopod crustacean, is an emerging model for cave biology. Cave and surface forms of this species differ in many characteristics, including eye size, pigmentation, and antennal length. Existing resources for this species include a linkage map, mapped regions responsible for eye and pigmentation traits, sequenced adult transcriptomes, and comparative embryological descriptions of the surface and cave forms. Our ultimate goal is to identify genes and mutations responsible for the differences between the cave and surface forms. To advance this goal, we decided to use a transcriptomic approach. Because many of these changes first appear during embryonic development, we sequenced embryonic transcriptomes of cave, surface, and hybrid individuals at the stage when eyes and pigment become evident in the surface form. We generated a cave, a surface, a hybrid, and an integrated transcriptome to identify differentially expressed genes in the cave and surface forms. Additionally, we identified genes with allele-specific expression in hybrid individuals. These embryonic transcriptomes are an important resource to assist in our ultimate goal of determining the genetic underpinnings of the divergence between the cave and surface forms.
Joshua B. Gross; Dennis A. Sun; Brian M. Carlson; Sivan Brodo-Abo; Meredith E. Protas. Developmental Transcriptomic Analysis of the Cave-Dwelling Crustacean, Asellus aquaticus. Genes 2019, 11, 42 .
AMA StyleJoshua B. Gross, Dennis A. Sun, Brian M. Carlson, Sivan Brodo-Abo, Meredith E. Protas. Developmental Transcriptomic Analysis of the Cave-Dwelling Crustacean, Asellus aquaticus. Genes. 2019; 11 (1):42.
Chicago/Turabian StyleJoshua B. Gross; Dennis A. Sun; Brian M. Carlson; Sivan Brodo-Abo; Meredith E. Protas. 2019. "Developmental Transcriptomic Analysis of the Cave-Dwelling Crustacean, Asellus aquaticus." Genes 11, no. 1: 42.
Cave animals are a fascinating group of species often demonstrating characteristics including reduced eyes and pigmentation, metabolic efficiency, and enhanced sensory systems.Asellus aquaticus, an isopod crustacean, is an emerging model for cave biology. Cave and surface forms of this species differ in many characteristics, including eye size, pigmentation and antennal length. Existing resources for this species include a linkage map, mapped regions responsible for eye and pigmentation traits, sequenced adult transcriptomes, and comparative embryological descriptions of the surface and cave forms. Our ultimate goal is to identify genes and mutations responsible for the differences between the cave and surface forms. To advance this goal, we decided to use a transcriptomic approach. Because many of these changes first appear during embryonic development, we sequenced embryonic transcriptomes of cave, surface, and hybrid individuals at the stage when eyes and pigment become evident in the surface form. We generated a cave, a surface, a hybrid, and an integrated transcriptome to identify differentially expressed genes in the cave and surface forms. Additionally, we identified genes with allele-specific expression in hybrid individuals. These embryonic transcriptomes are an important resource to assist in our ultimate goal of determining the genetic underpinnings of the divergence between the cave and surface forms.
Joshua B. Gross; Dennis A. Sun; Brian M. Carlson; Sivan Brodo-Abo; Meredith E. Protas. Developmental transcriptomic analysis of the cave-dwelling crustacean,Asellus aquaticus. 2019, 845990 .
AMA StyleJoshua B. Gross, Dennis A. Sun, Brian M. Carlson, Sivan Brodo-Abo, Meredith E. Protas. Developmental transcriptomic analysis of the cave-dwelling crustacean,Asellus aquaticus. . 2019; ():845990.
Chicago/Turabian StyleJoshua B. Gross; Dennis A. Sun; Brian M. Carlson; Sivan Brodo-Abo; Meredith E. Protas. 2019. "Developmental transcriptomic analysis of the cave-dwelling crustacean,Asellus aquaticus." , no. : 845990.
Organisms living in the subterranean biome evolve extreme characteristics including vision loss and sensory expansion. Despite prior work linking certain genes to Mendelian traits, the genetic basis for complex cave-associated traits remains unknown. Moreover, it is unclear if certain forms of genetic variation (e.g., indels, copy number variants) are more common in regressive evolution. Progress in this area has been limited by a lack of suitable natural model systems and genomic resources. In recent years, the Mexican tetra, Astyanax mexicanus, has advanced as a model for cave biology and regressive evolution. Here, we present the results of a genome-wide screen for in-frame indels using alignments of RNA-sequencing reads to the draft cavefish genome. Mutations were discovered in three genes associated with blood physiology (mlf1, plg, and wdr1), two genes associated with growth factor signaling (ghrb, rnf126), one gene linked to collagen defects (mia3), and one gene which may have a global epigenetic impact on gene expression (mki67). With one exception, polymorphisms were shared between Pachón and Tinaja cavefish lineages, and different from the surface-dwelling lineage. We confirmed the presence of mutations using direct Sanger sequencing and discovered remarkably similar developmental expression in both morphs despite substantial coding sequence alterations. Further, three mutated genes mapped near previously established quantitative trait loci associated with jaw size, condition factor, lens size, and neuromast variation. This work reveals previously unappreciated traits evolving in this species under environmental pressures (e.g., blood physiology) and provides insight to genetic changes underlying convergence of organisms evolving in complete darkness.
Daniel Berning; Hannah Adams; Heidi Luc; Joshua B Gross. In-Frame Indel Mutations in the Genome of the Blind Mexican Cavefish, Astyanax mexicanus. Genome Biology and Evolution 2019, 11, 2563 -2573.
AMA StyleDaniel Berning, Hannah Adams, Heidi Luc, Joshua B Gross. In-Frame Indel Mutations in the Genome of the Blind Mexican Cavefish, Astyanax mexicanus. Genome Biology and Evolution. 2019; 11 (9):2563-2573.
Chicago/Turabian StyleDaniel Berning; Hannah Adams; Heidi Luc; Joshua B Gross. 2019. "In-Frame Indel Mutations in the Genome of the Blind Mexican Cavefish, Astyanax mexicanus." Genome Biology and Evolution 11, no. 9: 2563-2573.
The complex geological history and tropical climate of Mesoamerica create a rich source of biodiversity from which we can study evolutionary processes. Here, we discuss highly divergent forms of lake-dwelling fishes distributed across southern Mexico and Central America, originally recognized as members of different genera (AstyanaxandBramocharax). Recent phylogenetic studies suggest these morphotypes group within the same genus and readily hybridize. Despite genetic similarities,Bramocharaxmorphs exhibit stark differences in cranial shape and dentition. We investigated the evolution of several cranial traits that vary across morphs collected from four lakes in Mexico and Nicaragua and discovered an ecomorphological cline from the northern to southern lakes. Northern populations of sympatric morphs exhibit similar cranial shape and tooth morphology. Southern populations ofBramocharax, however, have more maxillary teeth, larger unicuspid teeth, an elongated snout and a streamlined cranium compared toAstyanax. The divergence of craniofacial morphology in southern lakes likely evolved in response to environmental pressures. We discuss the ecological differences across the four lake systems in terms of geological history and trophic dynamics. In summary, our study suggests thatBramocharaxare likely locally-adapted members derived fromAstyanaxlineages, highlighting the complex evolutionary history of theAstyanaxgenus.
Amanda K. Powers; Carlos A. Garita-Alvarado; Rocio Rodiles-Hernández; Daniel J. Berning; Joshua B. Gross; Claudia Patricia Ornelas-García. A geographical cline in craniofacial morphology across populations of Mesoamerican lake-dwelling fishes. 2019, 684431 .
AMA StyleAmanda K. Powers, Carlos A. Garita-Alvarado, Rocio Rodiles-Hernández, Daniel J. Berning, Joshua B. Gross, Claudia Patricia Ornelas-García. A geographical cline in craniofacial morphology across populations of Mesoamerican lake-dwelling fishes. . 2019; ():684431.
Chicago/Turabian StyleAmanda K. Powers; Carlos A. Garita-Alvarado; Rocio Rodiles-Hernández; Daniel J. Berning; Joshua B. Gross; Claudia Patricia Ornelas-García. 2019. "A geographical cline in craniofacial morphology across populations of Mesoamerican lake-dwelling fishes." , no. : 684431.
In recent years, a draft genome for the blind Mexican cavefish (Astyanax mexicanus) has been released, revealing the sequence identities for thousands of genes. Prior research into this emerging model system capitalized on comprehensive genome-wide investigations that have identified numerous quantitative trait loci (QTL) associated with various cave-associated phenotypes. However, the ability to connect genes of interest to the heritable basis for phenotypic change remains a significant challenge. One technique that can facilitate deeper understanding of the role of development in troglomorphic evolution is whole-mount in situ hybridization. This technique can be implemented to directly compare gene expression between cave- and surface-dwelling forms, nominate candidate genes underlying established QTL, identify genes of interest from next-generation sequencing studies, or develop other discovery-based approaches. In this report, we present a simple protocol, supported by a flexible checklist, that can be widely adapted for use well beyond the presented study system. It is hoped that this protocol can serve as a broad resource for the Astyanax community and beyond.
Heidi Luc; Connor Sears; Andrew Raczka; Joshua B. Gross; Heid Luc. Wholemount In Situ Hybridization for Astyanax Embryos. Journal of Visualized Experiments 2019, e59114 .
AMA StyleHeidi Luc, Connor Sears, Andrew Raczka, Joshua B. Gross, Heid Luc. Wholemount In Situ Hybridization for Astyanax Embryos. Journal of Visualized Experiments. 2019; (145):e59114.
Chicago/Turabian StyleHeidi Luc; Connor Sears; Andrew Raczka; Joshua B. Gross; Heid Luc. 2019. "Wholemount In Situ Hybridization for Astyanax Embryos." Journal of Visualized Experiments , no. 145: e59114.
Natural model systems evolving under extreme environmental pressures provide the opportunity to advance our knowledge of how the craniofacial complex evolves in nature. Unlike traditional models, natural systems are less inbred, and therefore better model the complex variation of the human population. Owing to the nature of certain craniofacial aberrations in blind Mexican cavefish, we suggest that this organism can provide new insights to a variety of craniofacial changes. Diverse cranial features have evolved in natural cave‐dwelling Astyanax fish, which have thrived in the unforgiving darkness and nutrient‐poor environment of the cave for countless generations. While the genetic and environmental underpinnings of various cranial anomalies have been investigated for decades, a comprehensive characterization of their molecular and developmental origins remains incomplete. Cavefish provide numerous advantages given the availability of genomic resources, developmental and molecular tools, and the presence of a normative surface‐dwelling “ancestral” surrogate for comparative studies. By leveraging the frequency of abnormal and asymmetric cranial features in cavefish, we anticipate advances in our knowledge of the etiologies of irregular cranial features. Extreme adaptations in cavefish are expected to offer new insights into the complex and multifactorial nature of craniofacial disorders and facial asymmetry. This article is protected by copyright. All rights reserved.
Joshua B. Gross; Amanda K. Powers. A Natural Animal Model System of Craniofacial Anomalies: The Blind Mexican Cavefish. The Anatomical Record 2018, 303, 24 -29.
AMA StyleJoshua B. Gross, Amanda K. Powers. A Natural Animal Model System of Craniofacial Anomalies: The Blind Mexican Cavefish. The Anatomical Record. 2018; 303 (1):24-29.
Chicago/Turabian StyleJoshua B. Gross; Amanda K. Powers. 2018. "A Natural Animal Model System of Craniofacial Anomalies: The Blind Mexican Cavefish." The Anatomical Record 303, no. 1: 24-29.
Regressive evolution is a widespread phenomenon that affects every living organism, yet the mechanisms underlying trait loss remain largely unknown. Cave animals enable the study of degenerative disorders, owing to the frequent loss of eyes and pigmentation among lineages evolving in the subterranean habitat. Here, we utilize the blind Mexican cavefish, Astyanax mexicanus, to investigate regressive loss of pigmentation because “ancestral” surface-dwelling morphs allow direct comparisons with cave-dwelling forms. Two genes (Oca2-albinism and Mc1r-brown) have been linked to specific pigmentation alterations in several cavefish populations. Pigment cell (melanophore) number is a complex trait governed by multiple genes, and variation in this trait may contribute to pigmentation diversity in Astyanax. To uncover genes associated with this trait, we assembled a high-resolution linkage map and used automated phenotypic scoring to quantify melanophore number variation across seven body regions in a surface × Pachón cave F2 pedigree. QTL mapping yielded several markers strongly associated with melanophore number variation in the dorsal mid-lateral stripe area and superior head region, which anchor to regions of the Astyanax genome and the zebrafish genome. Within these syntenic regions, we identified two candidate genes, Tyrp1b and Pmela, with known roles in pigmentation based on gene ontology annotation. Mutant forms of these candidate genes in other organisms cause global and regional pigmentation variation, respectively. In Astyanax, these genes harbor coding sequence mutations and demonstrate differential expression in Pachón cavefish compared to surface morphs. In sum, this work identifies genes involved with complex aspects of Astyanax pigmentation and provides insight into genetic mechanisms governing regressive phenotypic change.
Bethany A. Stahl; Connor R. Sears; Li Ma; Molly Perkins; Joshua B. Gross. Pmela and Tyrp1b Contribute to Melanophore Variation in Mexican Cavefish. Origin and Evolution of Biodiversity 2018, 3 -22.
AMA StyleBethany A. Stahl, Connor R. Sears, Li Ma, Molly Perkins, Joshua B. Gross. Pmela and Tyrp1b Contribute to Melanophore Variation in Mexican Cavefish. Origin and Evolution of Biodiversity. 2018; ():3-22.
Chicago/Turabian StyleBethany A. Stahl; Connor R. Sears; Li Ma; Molly Perkins; Joshua B. Gross. 2018. "Pmela and Tyrp1b Contribute to Melanophore Variation in Mexican Cavefish." Origin and Evolution of Biodiversity , no. : 3-22.
Animal models provide useful tools for exploring the genetic basis of morphological, physiological and behavioral phenotypes. Cave-adapted species are particularly powerful models for a broad array of phenotypic changes with evolutionary, developmental and clinical relevance. Here, we explored the genetic underpinnings of previously characterized differences in locomotor activity patterns between the surface-dwelling and Pachón cave-dwelling populations ofAstyanax mexicanus.We identified multiple novel QTL underlying patterns in overall levels of activity (velocity), as well as spatial tank use (time spent near the top or bottom of the tank). Further, we demonstrated that different regions of the genome mediate distinct patterns in velocity and tank usage. We interrogated eight genomic intervals underlying these activity QTL distributed across six linkage groups. In addition, we employed transcriptomic data and draft genomic resources to generate and evaluate a list of 36 potential candidate genes. Interestingly, our data support the candidacy of a number of genes, but do not suggest that differences in the patterns of behavior observed here are the result of alterations to certain candidate genes described in other species (e.g., teleost multiple tissue opsins, melanopsins or members of the core circadian clockwork). This study expands our knowledge of the genetic architecture underlying activity differences in surface and cavefish. Future studies will help define the role of specific genes in shaping complex behavioral phenotypes inAstyanaxand other vertebrate taxa.
Brian M. Carlson; Ian B. Klingler; Bradley J. Meyer; Joshua B. Gross. Genetic analysis reveals candidate genes for activity QTL in the blind Mexican tetra,Astyanax mexicanus. PeerJ 2018, 6, e5189 .
AMA StyleBrian M. Carlson, Ian B. Klingler, Bradley J. Meyer, Joshua B. Gross. Genetic analysis reveals candidate genes for activity QTL in the blind Mexican tetra,Astyanax mexicanus. PeerJ. 2018; 6 ():e5189.
Chicago/Turabian StyleBrian M. Carlson; Ian B. Klingler; Bradley J. Meyer; Joshua B. Gross. 2018. "Genetic analysis reveals candidate genes for activity QTL in the blind Mexican tetra,Astyanax mexicanus." PeerJ 6, no. : e5189.
The precise mechanisms underlying cranial bone development, evolution and patterning remain incompletely characterised. This poses a challenge to understanding the etiologies of craniofacial malformations evolving in nature. Capitalising on natural variation, "evolutionary model systems" provide unique opportunities to identify underlying causes of aberrant phenotypes as a complement to studies in traditional systems. Mexican blind cavefish are a prime evolutionary model for cranial disorders since they frequently exhibit extreme alterations to the skull and lateral asymmetries. These aberrations occur in stark contrast to the normal cranial architectures of closely related surface-dwelling fish, providing a powerful comparative paradigm for understanding cranial bone formation. Using a longitudinal and in vivo analytical approach, we discovered two unusual ossification processes in cavefish that underlie the development of 'fragmented' and asymmetric cranial bones. The first mechanism involves the sporadic appearance of independent bony elements that fail to fuse together later in development. The second mechanism involves the "carving" of channels in the mature bone, a novel form of post-ossification remodeling. In the extreme cave environment, these novel mechanisms may have evolved to augment sensory input, and may indirectly result in a trade-off between sensory expansion and cranial bone development.
Amanda K. Powers; Shane A. Kaplan; Tyler Boggs; Joshua B. Gross. Facial bone fragmentation in blind cavefish arises through two unusual ossification processes. Scientific Reports 2018, 8, 7015 .
AMA StyleAmanda K. Powers, Shane A. Kaplan, Tyler Boggs, Joshua B. Gross. Facial bone fragmentation in blind cavefish arises through two unusual ossification processes. Scientific Reports. 2018; 8 (1):7015.
Chicago/Turabian StyleAmanda K. Powers; Shane A. Kaplan; Tyler Boggs; Joshua B. Gross. 2018. "Facial bone fragmentation in blind cavefish arises through two unusual ossification processes." Scientific Reports 8, no. 1: 7015.
Developmental patterning is a complex biological phenomenon, involving integrated cellular and molecular signaling across diverse tissues. In Astyanax cavefish, the lateral line sensory system is dramatically expanded in a region of the cranium marked by significant bone abnormalities. This system provides the opportunity to understand how facial bone patterning can become altered through sensory system changes. Here we investigate a classic postulation that mechanosensory receptor neuromasts seed intramembranous facial bones in aquatic vertebrates. Using an in vivo staining procedure across individual life history, we observed infraorbital canal neuromasts serving as sites of ossification for suborbital bones. The manner in which cavefish departed from the stereotypical and symmetrical canal neuromast patterns of closely-related surface-dwelling fish were associated with specific changes to the suborbital bone complex. For instance, bony fusion, rarely observed in surface fish, was associated with shorter distances between canal neuromasts in cavefish, suggesting that closer canal neuromasts result in bony fusions. Additionally, cavefish lacking the sixth suborbital bone (SO6) uniformly lacked the associated (sixth) canal neuromast. This study suggests that patterning of canal neuromasts may impact spatial position of suborbital bones across development. The absence of an eye and subsequent orbital collapse in cavefish appears to influence positional information normally inherent to the infraorbital canal. These alterations result in coordinated changes to adult neuromast and bone structures. This work highlights complex interactions between visual, sensory and bony tissues during development that explain certain abnormal craniofacial features in cavefish.
Amanda K. Powers; Tyler E. Boggs; Joshua B. Gross. Canal neuromast position prefigures developmental patterning of the suborbital bone series in Astyanax cave- and surface-dwelling fish. Developmental Biology 2018, 441, 252 -261.
AMA StyleAmanda K. Powers, Tyler E. Boggs, Joshua B. Gross. Canal neuromast position prefigures developmental patterning of the suborbital bone series in Astyanax cave- and surface-dwelling fish. Developmental Biology. 2018; 441 (2):252-261.
Chicago/Turabian StyleAmanda K. Powers; Tyler E. Boggs; Joshua B. Gross. 2018. "Canal neuromast position prefigures developmental patterning of the suborbital bone series in Astyanax cave- and surface-dwelling fish." Developmental Biology 441, no. 2: 252-261.
In this study, we report evidence of a novel duplication of Melanocortin receptor 1 (Mc1r) in the cavefish genome. This locus was discovered following the observation of excessive allelic diversity in a ∼820 bp fragment of Mc1r amplified via degenerate PCR from a natural population of Astyanax aeneus fish from Guerrero, Mexico. The cavefish genome reveals the presence of two closely related Mc1r open reading frames separated by a 1.46 kb intergenic region. One open reading frame corresponds to the previously reported Mc1r receptor, and the other open reading frame (duplicate copy) is 975 bp in length, encoding a receptor of 325 amino acids. Sequence similarity analyses position both copies in the syntenic region of the single Mc1r locus in 16 representative craniate genomes spanning bony fish (including Astyanax) to mammals, suggesting we discovered tandem duplicates of this important gene. The two Mc1r copies share ∼89% sequence similarity and, within Astyanax, are more similar to one another compared to other melanocortin family members. Future studies will inform the precise functional significance of the duplicated Mc1r locus and if this novel copy number variant may have adaptive significance for the Astyanax lineage.
Joshua B. Gross; James Weagley; Bethany A. Stahl; Li Ma; Luis Espinasa; Suzanne E. McGaugh. A local duplication of the Melanocortin receptor 1 locus in Astyanax. Genome 2018, 61, 254 -265.
AMA StyleJoshua B. Gross, James Weagley, Bethany A. Stahl, Li Ma, Luis Espinasa, Suzanne E. McGaugh. A local duplication of the Melanocortin receptor 1 locus in Astyanax. Genome. 2018; 61 (4):254-265.
Chicago/Turabian StyleJoshua B. Gross; James Weagley; Bethany A. Stahl; Li Ma; Luis Espinasa; Suzanne E. McGaugh. 2018. "A local duplication of the Melanocortin receptor 1 locus in Astyanax." Genome 61, no. 4: 254-265.