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The intestinal environment as an evolutionary adaptation to mouthbrooding in the Astatotilapia burtoni cichlid.

ABSTRACT: Many of the various parental care strategies displayed by animals are accompanied by a significant reduction in food intake that imposes a substantial energy trade-off. Mouthbrooding, as seen in several species of fish in which the parent holds the developing eggs and fry in the buccal cavity, represents an extreme example of reduced food intake during parental investment and is accompanied by a range of physiological adaptations. In this study we use 16S sequencing to characterize the gut microbiota of female Astatotilapia burtoni cichlid fish throughout the obligatory phase of self-induced starvation during the brooding cycle in comparison to stage-matched females that have been denied food for the same duration. In addition to a reduction of gut epithelial turnover, we find a dramatic reduction in species diversity in brooding stages that recovers upon release of fry and refeeding that is not seen in females that are simply starved. Based on overall species diversity as well as differential abundance of specific bacterial taxa, we suggest that rather than reflecting a simple deprivation of caloric intake, the gut microbiota is more strongly influenced by physiological changes specific to mouthbrooding including the reduced epithelial turnover and possible production of antimicrobial agents.

SUBMITTER: Faber-Hammond JJ

PROVIDER: S-EPMC7137464 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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The intestinal environment as an evolutionary adaptation to mouthbrooding in the Astatotilapia burtoni cichlid.

Faber-Hammond Josh J JJ Coyle Kaitlin P KP Bacheller Shannon K SK Roberts Cameron G CG Mellies Jay L JL Roberts Reade B RB Renn Suzy C P SCP

FEMS microbiology ecology 20190301 3

Many of the various parental care strategies displayed by animals are accompanied by a significant reduction in food intake that imposes a substantial energy trade-off. Mouthbrooding, as seen in several species of fish in which the parent holds the developing eggs and fry in the buccal cavity, represents an extreme example of reduced food intake during parental investment and is accompanied by a range of physiological adaptations. In this study we use 16S sequencing to characterize the gut micro ...[more]

PMID: 30753545

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Project description:BACKGROUND:Parental care, while increasing parental fitness through offspring survival, also bears cost to the care-giving parent. Consequentially, trade offs between parental care and other vitally important traits, such as the immune system seem evident. In co-occurring phases of parental care and immunological challenges negative consequences through a resource allocation trade off on both the parental and the offspring conditions can be predicted. While the immune system reflects parental stress conditions, parental immunological investments also boost offspring survival via the transfer of immunological substances (trans-generational immune priming). We investigated this relationship in the mouthbrooding East African cichlid Astotatilapia burtoni. Prior to mating, females were exposed to an immunological activation, while others remained immunologically naïve. Correspondingly, the immunological status of females was either examined directly after reproduction or after mouthbrooding had ceased. Offspring from both groups were exposed to immunological challenges to assess the extent of trans-generational immune priming. As proxy for immune status, cellular immunological activity and gene expression were determined. RESULTS:Both reproducing and mouthbrooding females allocate their resources towards reproduction. While upon reproduction the innate immune system was impeded, mouthbrooding females showed an attenuation of inflammatory components. Juveniles from immune challenged mouthbrooding females showed downregulation of immune and life history candidate genes, implying a limitation of trans-generational plasticity when parents experience stress during the costly reproductive phase. CONCLUSION:Our results provide evidence that both parental investment via mouthbrooding and the rise of the immunological activity upon an immune challenge are costly traits. If applied simultaneously, not only mothers seem to be impacted in their performance, but also offspring are impeded in their ability to react upon a potentially virulent pathogen exposure.

Project description:BackgroundCichlid fishes have evolved remarkably diverse reproductive, social, and feeding behaviors. Cell-to-cell signaling molecules, notably neuropeptides and peptide hormones, are known to regulate these behaviors across vertebrates. This class of signaling molecules derives from prohormone genes that have undergone multiple duplications and losses in fishes. Whether and how subfunctionalization, neofunctionalization, or losses of neuropeptides and peptide hormones have contributed to fish behavioral diversity is largely unknown. Information on fish prohormones has been limited and is complicated by the whole genome duplication of the teleost ancestor. We combined bioinformatics, mass spectrometry-enabled peptidomics, and molecular techniques to identify the suite of neuropeptide prohormones and pituitary peptide products in Astatotilapia burtoni, a well-studied member of the diverse African cichlid clade.ResultsUtilizing the A. burtoni genome, we identified 148 prohormone genes, with 21 identified as a single copy and 39 with at least 2 duplicated copies. Retention of prohormone duplicates was therefore 41 %, which is markedly above previous reports for the genome-wide average in teleosts. Beyond the expected whole genome duplication, differences between cichlids and mammals can be attributed to gene loss in tetrapods and additional duplication after divergence. Mass spectrometric analysis of the pituitary identified 620 unique peptide sequences that were matched to 120 unique proteins. Finally, we used in situ hybridization to localize the expression of galanin, a prohormone with exceptional sequence divergence in cichlids, as well as the expression of a proopiomelanocortin, prohormone that has undergone an additional duplication in some bony fish lineages.ConclusionWe characterized the A. burtoni prohormone complement. Two thirds of prohormone families contain duplications either from the teleost whole genome duplication or a more recent duplication. Our bioinformatic and mass spectrometric findings provide information on a major vertebrate clade that will further our understanding of the functional ramifications of these prohormone losses, duplications, and sequence changes across vertebrate evolution. In the context of the cichlid radiation, these findings will also facilitate the exploration of neuropeptide and peptide hormone function in behavioral diversity both within A. burtoni and across cichlid and other fish species.

Dataset Information

The intestinal environment as an evolutionary adaptation to mouthbrooding in the Astatotilapia burtoni cichlid.

Publications

The intestinal environment as an evolutionary adaptation to mouthbrooding in the Astatotilapia burtoni cichlid.

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