Evolutionary patterns of diadromy in fishes: more than a transitional state between marine and freshwater.

Background: Across the tree of life there are numerous evolutionary transitions between different habitats (i.e., aquatic and terrestrial or marine and freshwater). Many of these dramatic evolutionary shifts parallel developmental shifts that require physiological, anatomical and behavioral changes for survival and reproduction. Diadromy (scheduled movement between marine and freshwater) has been characterized as a behavior that acts as an evolutionary intermediate state between marine and freshwater environments, implying that diadromous lineages are evolutionarily transient. This hypothesis comes with assumptions regarding the rates of evolutionary transitions in and out of diadromy as well as rates of speciation and extinction in diadromous fishes.

Results: Based on a published phylogeny of 7822 species of ray-finned fishes, state speciation and extinction models of evolutionary transition between marine, freshwater, and diadromous species suggest transition rates out of diadromy are 5-100 times higher that transition between marine and freshwater or into diadromy. Additionally, high speciation and low extinction rates separate diadromous fishes from marine and freshwater species. As a result, net diversification (net diversification = speciation - extinction) is about 7-40 times higher in diadromous fishes compared to freshwater and marine respectively. Together the transition, speciation, and extinction rates suggest diadromy is the least stable of the three states.

Conclusion: Evolutionary transitions to diadromy are rare in fishes. However, once established, diversification rates in diadromous lineages are high compared to both marine and freshwater species. Diadromous lineages tend to be more transient than marine or freshwater lineages and are found to give rise to marine and freshwater specialists in addition to diadromous descendants. Although diadromy is not a necessary evolutionary intermediate between marine and freshwater, these results support the interpretation of diadromy as an important, occasionally intermediate state, that contributes to biodiversity in fishes in all environments. This evolutionary instability of diadromous lineages is counteracted by their relatively high diversification rates. These findings highlight the importance of integrating the dynamics of diversification and major evolutionary transitions for understanding macroevolutionary patterns.