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Ahi, E. P., Duenser, A., Singh, P., Gessl, W. & Sturmbauer, C. (2020). Appetite regulating genes may contribute to herbivory versus carnivory trophic divergence in haplochromine cichlids. PeerJ, 8, Article ID e8375.
Open this publication in new window or tab >>Appetite regulating genes may contribute to herbivory versus carnivory trophic divergence in haplochromine cichlids
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2020 (English)In: PeerJ, ISSN 2167-8359, E-ISSN 2167-8359, Vol. 8, article id e8375Article in journal (Refereed) Published
Abstract [en]

Feeding is a complex behaviour comprised of satiety control, foraging, ingestion and subsequent digestion. Cichlids from the East African Great Lakes are renowned for their diverse trophic specializations, largely predicated on highly variable jaw morphologies. Thus, most research has focused on dissecting the genetic, morphological and regulatory basis of jaw and teeth development in these species. Here for the first time we explore another aspect of feeding, the regulation of appetite related genes that are expressed in the brain and control satiety in cichlid fishes. Using qPCR analysis, we first validate stably expressed reference genes in the brain of six haplochromine cichlid species at the end of larval development prior to foraging. We next evaluate the expression of 16 appetite related genes in herbivorous and carnivorous species from the parallel radiations of Lake Tanganyika, Malawi and Victoria. Interestingly, we find increased expression of two appetite-regulating genes (anorodgenic genes), cart and npy2r, in the brain of carnivorous species in all the three lakes. This supports the notion that appetite gene regulation might play a part in determining trophic niche specialization in divergent cichlid species, already prior to exposure to different diets. Our study contributes to the limited body of knowledge on the neurological circuitry that controls feeding transitions and adaptations in cichlids and other teleosts.

Place, publisher, year, edition, pages
PEERJ INC, 2020
Keywords
Appetite regulation, East African Lakes, Cichlids, Gene expression, Trophic specialization, Adaptive radiation, Anorexigenic, Orexigenic, Brain, Larval development
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-406179 (URN)10.7717/peerj.8375 (DOI)000508429200006 ()31998557 (PubMedID)
Available from: 2020-03-06 Created: 2020-03-06 Last updated: 2020-03-06Bibliographically approved
Ahi, E. P., Lecaudey, L. A., Ziegelbecker, A., Steiner, O., Glabonjat, R., Goessler, W., . . . Sefc, K. M. (2020). Comparative transcriptomics reveals candidate carotenoid color genes in an East African cichlid fish. BMC Genomics, 21, Article ID 54.
Open this publication in new window or tab >>Comparative transcriptomics reveals candidate carotenoid color genes in an East African cichlid fish
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2020 (English)In: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 21, article id 54Article in journal (Refereed) Published
Abstract [en]

Background: Carotenoids contribute significantly to animal body coloration, including the spectacular color pattern diversity among fishes. Fish, as other animals, derive carotenoids from their diet. Following uptake, transport and metabolic conversion, carotenoids allocated to body coloration are deposited in the chromatophore cells of the integument. The genes involved in these processes are largely unknown. Using RNA-Sequencing, we tested for differential gene expression between carotenoid-colored and white skin regions of a cichlid fish, Tropheus duboisi "Maswa", to identify genes associated with carotenoid-based integumentary coloration. To control for positional gene expression differences that were independent of the presence/absence of carotenoid coloration, we conducted the same analyses in a closely related population, in which both body regions are white.

Results: A larger number of genes (n = 50) showed higher expression in the yellow compared to the white skin tissue than vice versa (n = 9). Of particular interest was the elevated expression level of bco2a in the white skin samples, as the enzyme encoded by this gene catalyzes the cleavage of carotenoids into colorless derivatives. The set of genes with higher expression levels in the yellow region included genes involved in xanthophore formation (e.g., pax7 and sox10), intracellular pigment mobilization (e.g., tubb, vim, kif5b), as well as uptake (e.g., scarb1) and storage (e.g., plin6) of carotenoids, and metabolic conversion of lipids and retinoids (e.g., dgat2, pnpla2, akr1b1, dhrs). Triglyceride concentrations were similar in the yellow and white skin regions. Extracts of integumentary carotenoids contained zeaxanthin, lutein and beta-cryptoxanthin as well as unidentified carotenoid structures.

Conclusion: Our results suggest a role of carotenoid cleavage by Bco2 in fish integumentary coloration, analogous to previous findings in birds. The elevated expression of genes in carotenoid-rich skin regions with functions in retinol and lipid metabolism supports hypotheses concerning analogies and shared mechanisms between these metabolic pathways. Overlaps in the sets of differentially expressed genes (including dgat2, bscl2, faxdc2 and retsatl) between the present study and previous, comparable studies in other fish species provide useful hints to potential carotenoid color candidate genes.

Place, publisher, year, edition, pages
BMC, 2020
Keywords
Carotenoids, Body coloration, Color genes, Gene expression, Cichlidae, Tropheus, Lipids, RNA-Seq, BCO2
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-409786 (URN)10.1186/s12864-020-6473-8 (DOI)000521340900004 ()31948394 (PubMedID)
Available from: 2020-05-04 Created: 2020-05-04 Last updated: 2020-05-04Bibliographically approved
Ahi, E. P., Singh, P., Duenser, A., Gessl, W. & Sturmbauer, C. (2019). Divergence in larval jaw gene expression reflects differential trophic adaptation in haplochromine cichlids prior to foraging. BMC Evolutionary Biology, 19, Article ID 150.
Open this publication in new window or tab >>Divergence in larval jaw gene expression reflects differential trophic adaptation in haplochromine cichlids prior to foraging
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2019 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 19, article id 150Article in journal (Refereed) Published
Abstract [en]

BackgroundUnderstanding how variation in gene expression contributes to morphological diversity is a major goal in evolutionary biology. Cichlid fishes from the East African Great lakes exhibit striking diversity in trophic adaptations predicated on the functional modularity of their two sets of jaws (oral and pharyngeal). However, the transcriptional basis of this modularity is not so well understood, as no studies thus far have directly compared the expression of genes in the oral and pharyngeal jaws. Nor is it well understood how gene expression may have contributed to the parallel evolution of trophic morphologies across the replicate cichlid adaptive radiations in Lake Tanganyika, Malawi and Victoria.ResultsWe set out to investigate the role of gene expression divergence in cichlid fishes from these three lakes adapted to herbivorous and carnivorous trophic niches. We focused on the development stage prior to the onset of exogenous feeding that is critical for understanding patterns of gene expression after oral and pharyngeal jaw skeletogenesis, anticipating environmental cues. This framework permitted us for the first time to test for signatures of gene expression underlying jaw modularity in convergent eco-morphologies across three independent adaptive radiations. We validated a set of reference genes, with stable expression between the two jaw types and across species, which can be important for future studies of gene expression in cichlid jaws. Next we found evidence of modular and non-modular gene expression between the two jaws, across different trophic niches and lakes. For instance, prdm1a, a skeletogenic gene with modular anterior-posterior expression, displayed higher pharyngeal jaw expression and modular expression pattern only in carnivorous species. Furthermore, we found the expression of genes in cichlids jaws from the youngest Lake Victoria to exhibit low modularity compared to the older lakes.ConclusionOverall, our results provide cross-species transcriptional comparisons of modularly-regulated skeletogenic genes in the two jaw types, implicating expression differences which might contribute to the formation of divergent trophic morphologies at the stage of larval independence prior to foraging.

Place, publisher, year, edition, pages
BMC, 2019
Keywords
Haplochromine cichlids, Modularity, jaw development, Trophic specialization, Adaptive radiation, East African lakes
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-391368 (URN)10.1186/s12862-019-1483-3 (DOI)000477028400003 ()31340758 (PubMedID)
Available from: 2019-09-04 Created: 2019-09-04 Last updated: 2019-09-04Bibliographically approved
Ahi, E. P., Richter, F., Lecaudey, L. A. & Sefc, K. M. (2019). Gene expression profiling suggests differences in molecular mechanisms of fin elongation between cichlid species. Scientific Reports, 9, Article ID 9052.
Open this publication in new window or tab >>Gene expression profiling suggests differences in molecular mechanisms of fin elongation between cichlid species
2019 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 9, article id 9052Article in journal (Refereed) Published
Abstract [en]

Comparative analyses of gene regulation inform about the molecular basis of phenotypic trait evolution. Here, we address a fin shape phenotype that evolved multiple times independently across teleost fish, including several species within the family Cichlidae. In a previous study, we proposed a gene regulatory network (GRN) involved in the formation and regeneration of conspicuous filamentous elongations adorning the unpaired fins of the Neolamprologus brichardi. Here, we tested the members of this network in the blockhead cichlid, Steatocranus casuarius, which displays conspicuously elongated dorsal and moderately elongated anal fins. Our study provided evidence for differences in the anatomy of fin elongation and suggested gene regulatory divergence between the two cichlid species. Only a subset of the 20 genes tested in S. casuarius showed the qPCR expression patterns predicted from the GRN identified in N. brichardi, and several of the gene-by-gene expression correlations differed between the two cichlid species. In comparison to N. brichardi, gene expression patterns in S. casuarius were in better (but not full) agreement with gene regulatory interactions inferred in zebrafish. Within S. casuarius, the dorsoventral asymmetry in ornament expression was accompanied by differences in gene expression patterns, including potential regulatory differentiation, between the anal and dorsal fin.

Place, publisher, year, edition, pages
Nature Publishing Group, 2019
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-390679 (URN)10.1038/s41598-019-45599-w (DOI)000472477700007 ()31227799 (PubMedID)
Available from: 2019-08-15 Created: 2019-08-15 Last updated: 2019-08-15Bibliographically approved
Lecaudey, L. A., Sturmbauer, C., Singh, P. & Ahi, E. P. (2019). Molecular mechanisms underlying nuchal hump formation in dolphin cichlid, Cyrtocara moorii. Scientific Reports, 9, Article ID 20296.
Open this publication in new window or tab >>Molecular mechanisms underlying nuchal hump formation in dolphin cichlid, Cyrtocara moorii
2019 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 9, article id 20296Article in journal (Refereed) Published
Abstract [en]

East African cichlid fishes represent a model to tackle adaptive changes and their connection to rapid speciation and ecological distinction. In comparison to bony craniofacial tissues, adaptive morphogenesis of soft tissues has been rarely addressed, particularly at the molecular level. The nuchal hump in cichlids fishes is one such soft-tissue and exaggerated trait that is hypothesized to play an innovative role in the adaptive radiation of cichlids fishes. It has also evolved in parallel across lakes in East Africa and Central America. Using gene expression profiling, we identified and validated a set of genes involved in nuchal hump formation in the Lake Malawi dolphin cichlid, Cyrtocara moorii. In particular, we found genes differentially expressed in the nuchal hump, which are involved in controlling cell proliferation (btg3, fosl1a and pdgfrb), cell growth (dlk1), craniofacial morphogenesis (dlx5a, mycn and tcf12), as well as regulators of growth-related signals (dpt, pappa and socs2). This is the first study to identify the set of genes associated with nuchal hump formation in cichlids. Given that the hump is a trait that evolved repeatedly in several African and American cichlid lineages, it would be interesting to see if the molecular pathways and genes triggering hump formation follow a common genetic track or if the trait evolved in parallel, with distinct mechanisms, in other cichlid adaptive radiations and even in other teleost fishes.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2019
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-406195 (URN)10.1038/s41598-019-56771-7 (DOI)000508984900015 ()31889116 (PubMedID)
Available from: 2020-03-05 Created: 2020-03-05 Last updated: 2020-03-05Bibliographically approved
Ahi, E. P., Brunel, M., Tsakoumis, E. & Schmitz, M. (2019). Transcriptional study of appetite regulating genes in the brain of zebrafish (Danio rerio) with impaired leptin signalling. Scientific Reports, 9, Article ID 20166.
Open this publication in new window or tab >>Transcriptional study of appetite regulating genes in the brain of zebrafish (Danio rerio) with impaired leptin signalling
2019 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 9, article id 20166Article in journal (Refereed) Published
Abstract [en]

The hormone leptin is a key regulator of body weight, food intake and metabolism. In mammals, leptin acts as an anorexigen and inhibits food intake centrally by affecting the appetite centres in the hypothalamus. In teleost fish, the regulatory connections between leptin and other appetite-regulating genes are largely unknown. In the present study, we used a zebrafish mutant with a loss of function leptin receptor to investigate brain expression patterns of 12 orexigenic and 24 anorexigenic genes under different feeding conditions (normal feeding, 7-day fasting, 2 and 6-hours refeeding). Expression patterns were compared to wild-type zebrafish, in order to identify leptin-dependent differentially expressed genes under different feeding conditions. We provide evidence that the transcription of certain orexigenic and anorexigenic genes is influenced by leptin signalling in the zebrafish brain. We found that the expression of orexigenic genes was not affected by impaired leptin signalling under normal feeding conditions; however, several orexigenic genes showed increased transcription during fasting and refeeding, including agrp, apln, galr1a and cnr1. This suggests an inhibitory effect of leptin signal on the transcription of these orexigenic genes during short-term fasting and refeeding in functional zebrafish. Most pronounced effects were observed in the group of anorexigenic genes, where the impairment of leptin signalling resulted in reduced gene expression in several genes, including cart family, crhb, gnrh2, mc4r, pomc and spx, in the control group. This suggests a stimulatory effect of leptin signal on the transcription of these anorexigenic genes under normal feeding condition. In addition, we found multiple gain and loss in expression correlations between the appetite-regulating genes, in zebrafish with impaired leptin signal, suggesting the presence of gene regulatory networks downstream of leptin signal in zebrafish brain. The results provide the first evidence for the effects of leptin signal on the transcription of various appetite-regulating genes in zebrafish brain, under different feeding conditions. Altogether, these transcriptional changes suggest an anorexigenic role for leptin signal, which is likely to be mediated through distinct set of appetite-regulating genes under different feeding conditions.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2019
National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-406458 (URN)10.1038/s41598-019-56779-z (DOI)000509342200002 ()31882937 (PubMedID)
Available from: 2020-03-09 Created: 2020-03-09 Last updated: 2020-03-09Bibliographically approved
Ahi, E. P., Singh, P., Lecaudey, L. A., Gessl, W. & Sturmbauer, C. (2018). Maternal mRNA input of growth and stress-response-related genes in cichlids in relation to egg size and trophic specialization. EvoDevo, 9, Article ID 23.
Open this publication in new window or tab >>Maternal mRNA input of growth and stress-response-related genes in cichlids in relation to egg size and trophic specialization
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2018 (English)In: EvoDevo, ISSN 2041-9139, E-ISSN 2041-9139, Vol. 9, article id 23Article in journal (Refereed) Published
Abstract [en]

Background: Egg size represents an important form of maternal effect determined by a complex interplay of long-term adaptation and short-term plasticity balancing egg size with brood size. Haplochromine cichlids are maternal mouthbrooders showing differential parental investment in different species, manifested in great variation in egg size, brood size and duration of maternal care. Little is known about maternally determined molecular characters of eggs in fishes and their relation to egg size and trophic specialization. Here we investigate maternal mRNA inputs of selected growth- and stress-related genes in eggs of mouthbrooding cichlid fishes adapted to different trophic niches from Lake Tanganyika, Lake Malawi, Lake Victoria and compare them to their riverine allies.

Results: We first identified two reference genes, atf7ip and mid1ip1, to be suitable for cross-species quantification of mRNA abundance via qRT-PCR in the cichlid eggs. Using these reference genes, we found substantial variation in maternal mRNA input for a set of candidate genes related to growth and stress response across species and lakes. We observed negative correlation of mRNA abundance between two of growth hormone receptor paralogs (ghr1 and ghr2) across all haplochromine cichlid species which also differentiate the species in the two younger lakes, Malawi and Lake Victoria, from those in Lake Tanganyika and ancestral riverine species. Furthermore, we found correlations between egg size and maternal mRNA abundance of two growth-related genes igf2 and ghr2 across the haplochromine cichlids as well as distinct clustering of the species based on their trophic specialization using maternal mRNA abundance of five genes (ghr1, ghr2, igf2, gr and sgk1).

Conclusions: These findings indicate that variations in egg size in closely related cichlid species can be linked to differences in maternal RNA deposition of key growth-related genes. In addition, the cichlid species with contrasting trophic specialization deposit different levels of maternal mRNAs in their eggs for particular growth-related genes; however, it is unclear whether such differences contribute to differential morphogenesis at later stages of development. Our results provide first insights into this aspect of gene activation, as a basis for future studies targeting their role during ecomorphological specialization and adaptive radiation.

Place, publisher, year, edition, pages
BMC, 2018
Keywords
Haplochromine cichlids, Maternal mRNA, Eggs, Trophic specialization, Adaptive radiation, East African lakes
National Category
Evolutionary Biology Zoology
Identifiers
urn:nbn:se:uu:diva-372382 (URN)10.1186/s13227-018-0112-3 (DOI)000451770100001 ()30519389 (PubMedID)
Available from: 2019-01-07 Created: 2019-01-07 Last updated: 2019-01-07Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-6528-1187

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