How mouthbrooding cichlid mothers avoid consuming their brood

Abstract

When offspring number in the tens or hundreds, fish had to get inventive to keep them safe and a few came up with one ingenious strategy: they hold their eggs in their mouths until the youngsters hatch. ‘Mouthbrooding is an adaptation in response to predation pressure’, says Suzy Renn from Reed College, USA. But, when cichlid (Astatotilapia burtoni) mothers gather their eggs into their mouths, dining is off the menu for 2–3 weeks, which takes its toll. The mothers lose weight (body mass) until they regain the ability to eat – once the fry are liberated – and they begin preparing for their next clutch. All of this is tightly coordinated by circuits in the brain, but exactly which neurotransmitters and hormones are key to the precise regulation of the fish's behaviour wasn't clear. Renn and Joshua Faber-Hammond, also from Reed College, monitored the brains of mouthbrooding cichlid mothers to find out which genes were activated at different stages of the process to coordinate the physical changes that accompany cichlid parenthood.Renn collected samples of the A. burtoni mothers’ brains 2 days after spawning when their eggs were fresh in their mouths, 14 days after spawning when the fry were almost ready for release, 2 days after the fry had been set free and 14 days after fry release, when the mothers were preparing to lay another clutch. Then, Faber-Hammond analysed the brain mRNA, which is produced when a gene is expressed for protein production, to identify which genes are activated when the mothers go without food while brooding their young and afterwards, during recovery.Identifying 128 genes whose abundance varied as the fish progressed through their parenting odyssey, it was clear that genes involved in controlling when animals become more nurturing, when they feed and metabolic activity all played essential roles at different stages. Most impressively, the gene expression levels of two neuropeptides – neurotensin and galanin, both of which impact the bond between parent and young in various creatures – which had been high when the fry were in the mother's mouth, plummeted after mothers released their offspring. ‘That could mean that the signals in the brain that increase parental care in fish may be some of the same signals that increase parental care in frogs, birds and even mice’, says Renn, explaining that the reductions are probably associated with the mothers gearing up to protect their young once free.Genes that are involved in regulating appetite also featured large, with genes for hormones and neuropeptides that supress appetite surging when the mothers were mouthbrooding, while the expression of hormones that stimulate appetite increased once they could resume feeding after releasing their young. However, some appetite-stimulating genes increased their activity while the mothers were brooding, which ‘underscores the complexity of feeding regulation under a situation of voluntary starvation’, says Renn.The duo also noticed that genes that encode proteins involved in energy production became more active when the mothers were fasting, in addition to genes that are known to turn down metabolism in fasting or hibernating creatures. ‘That we see these changes … occurring in brain samples may reflect high metabolic demand of neural tissue’, says Renn. Meanwhile, the expression of genes that encode proteins that carry oxygen plummeted toward the end of mouthbrooding, while expression of those encoding proteins that protect the brain from damage rocketed.‘The gene expression patterns reveal how the female brain may resolve trade-offs between metabolic demands and parental care’, says Renn, adding that many of the changes found in the brain probably also occur in the bodies of the mouthbrooding mothers.