Climate changes driving fusuline macroevolution

There has been long-standing debate about what environmental factors are the main drivers of biodiversity changes. During the last hundreds of years, there are convincing signs that rising and falling CO₂ and temperatures are affecting both marine and terrestrial biodiversities. However, this has been rarely tested with high-resolution biodiversity changes in deep time. It is also difficult to judge whether the current diversity loss caused by global changes is a long-term tendency or a catastrophic event because the observatory records are too short to predict the future. Fusuline foraminifers were a major group of Carboniferous through Permian marine microorganisms for ~91.8 million years (Myr) during which they experienced changes from icehouse to greenhouse climates. Here we use a high-resolution analysis of fusuline diversity with an average resolution 40 thousand years (kyr) to analyze their speciation and extinction dynamics at multiple temporal levels during this interval of major climatic shifts. This new database encompasses 1391 species from 293 published stratigraphic sections worldwide using constrained optimization method (CONOP). Our results show a symmetric diversity pattern with a peak between 295.24 Ma and 293.57 Ma in the middle of the lifespan of Fusulinida and temporally coincident with the apex of the Late Paleozoic ice age (LPIA). The shift from icehouse to greenhouse climates led to the decline of fusuline diversity. Major disruptions in fusuline diversity are found during the late Moscovian-Kasimovian interglacial event, the post-LPIA long-term warming and the middle-late Guadalupian extinction before the clade was eliminated by the end-Permian mass extinction (EPME). Each of the events of large diversity loss are linked to global warming, probably induced by massive release of greenhouse gases from intensive volcanism. The high temporal resolution also allows us to interrogate the finer-scale patterns revealing that species richness, origination, and extinction rates were paced by long-term astronomical forcing, including ~1.0 Myr obliquity and ~2.1 Myr eccentricity cycles. This highlights the substantial role of astronomically forced climate variability on the rhythms of biological evolution. Our study suggests climatic forcing of long-term changes and catastrophic events in fusuline diversity, with global cooling fueling foraminifera diversifications. This pattern is consistent with the late Cenozoic diversifications of recent foraminifera before the mid-Pliocene warming period.