Behaviour drives morphology: voluntary emersion patterns shape gill structure in genetically identical mangrove rivulus

The self-fertilizing mangrove rivulus, Kryptolebias marmoratus, can produce homozygous ‘clonal’ offspring and are highly tolerant of severe environmental conditions, including air exposure (emersion) for weeks at a time. We tested the following hypotheses: (1) individual fish that voluntarily emerse more possess gill and skin features better suited for life on land than fish that emerse less often, and (2) individual differences in emersion tendencies cause these morphological changes. We predicted that individuals spending more time in air would have a reduced gill surface area (shorter, thicker gill lamellae and well developed interlamellar cell masses (ILCM)) and a thicker cutaneous epidermis compared to fish preferring to remain in water. These differences were predicted to disappear if fish were prevented from emersing and predicted to reappear if fish were once again allowed to emerse. Fish were videorecorded for 7 days while voluntarily moving between aquatic and terrestrial habitats to determine individual emersion tendencies. We prevented a subset of fish from emersing for 7 days, and then allowed a subset of these fish to emerse for a final 7 days. We found that individual fish spent anywhere from 0 to 78% of the time emersing. Emersion time was positively correlated with gill ILCM height, but not with any other morphological feature. There was no relationship between ILCM height and emersion time after fish were prevented from emersing for 7 days, but this relationship reappeared when fish were once again able to emerse. These results indicate that genetically identical K. marmoratus show highly variable behavioural phenotypes that influence gill remodelling. Fish that voluntarily spend more time emersed reduce gill surface area, a modification that may limit branchial water loss and provide support for gill lamellae. This is the first report of respiratory morphologies linked to variation in behavioural phenotype.