The true tempo of evolutionary radiation and decline revealed on the Hawaiian archipelago

Abstract

Establishing the relationship between rates of change in species richness and biotic and abiotic environmental change is a major goal of evolutionary biology. Although exquisite fossil and geological records provide insight in rare cases, most groups lack high-quality fossil records. Consequently, biologists typically rely on molecular phylogenies to study the diversity dynamics of clades, usually by correlating changes in diversification rate with environmental or trait shifts. However, inferences drawn from molecular phylogenies can be limited owing to the challenge of accounting for extinct species, making it difficult to accurately determine the underlying diversity dynamics that produce them. Here, using a geologically informed model of the relationship between changing island area and species richness for the Hawaiian archipelago, we infer the rates of species richness change for 14 endemic groups over their entire evolutionary histories without the need for fossil data, or molecular phylogenies. We find that these endemic clades underwent evolutionary radiations characterized by initially increasing rates of species accumulation, followed by slow-downs. In fact, for most groups on most islands, their time of evolutionary expansion has long past, and they are now undergoing previously unrecognized long-term evolutionary decline. Our results show how landscape dynamism can drive evolutionary dynamics over broad timescales, including driving species loss that is not readily detected using molecular phylogenies, or without a rich fossil record. We anticipate that examination of other clades where the relationship between environmental change and species richness change can be quantified will reveal that many other living groups have also experienced similarly complex evolutionary trajectories, including long-term and ongoing evolutionary decline.