Sorting of persistent morphological polymorphisms links paleobiological pattern to population process

Abstract Biological variation fuels evolutionary change. Across longer timescales, however, polymorphisms at both the genomic and phenotypic levels often persists longer than would be expected under standard population genetic models such as positive selection or genetic drift. Explaining the maintenance of this variation within populations across long timespans via balancing selection has been a major triumph of theoretical population genetics and ecology. Although persistent polymorphisms can often be traced in fossil lineages over long periods through the rock record, paleobiology has had little to say about either the long-term maintenance of phenotypic variation or its macroevolutionary consequences. I explore the dynamics that occur when persistent polymorphisms maintained over long lineage durations are filtered into descendant lineages during periods of demographic upheaval that occur at speciation. I evaluate these patterns in two lineages: Ectocion , a genus of Eocene mammals, and botryocrinids, a Mississippian cladid crinoid family. Following origination, descendants are less variable than their ancestors. The patterns by which ancestral variation is sorted cannot be distinguished from drift. Maintained and accumulated polymorphisms in highly variable ancestral lineages such as Barycrinus rhombiferus (Owen and Shumard 1852) may fuel radiations as character states are sorted into multiple descendant lineages. Interrogating the conditions under which trans-specific polymorphism is either maintained or lost during periods of demographic and ecological upheaval can explain how population-level processes contribute to the emergent macroevolutionary dynamics that shape the history of life as preserved in the fossil record. Non-technical abstract Understanding how morphological variation changes within populations over relatively short timescales in response to environmental changes and ecology (i.e., thousands of years) is a major focus of paleontology and evolutionary biology. A distinct focus is in understanding the broad-scale patterns by which lineages have diversified into distinct environments over geologic time (i.e., millions of years). One major challenge has been reconciling how and whether processes acting over shorter timescales shape the patterns observed over long timescales. One way of examining morphological variation at the population level is by examining the distribution of polymorphic character states--discrete anatomical features that vary within a population. Fossil species often maintain such polymorphisms for long periods of time, with such variation even sometimes inherited by new species from their ancestors. In this article, I suggest that examining how these polymorphisms are distributed among incipient descendant lineages might help link the ecological and evolutionary processes that act at the population level (e.g., natural selection, genetic drift, competition, predation) to the paleobiological patterns that are often reconstructed across many species and over long timescales. I explore these dynamics in two lineages: Ectocion , a genus of Eocene mammals, and botryocrinids, a Mississippian cladid crinoid family. I found that new lineages typically have fewer polymorphisms than their ancestors, suggesting that ancestral variation is “sorted” into incipient lineages during speciation. This variation appears to be sorted randomly, which means that it is not possible to detect the influence of natural selection in guiding the inheritance of ancestral morphologies. I suggest that the patterns by which ancestral variation is sorted into new species may explain patterns of lineage diversification over long timescales, highlighting how population processes can extend their influence over longer timescales to shape large-scale evolutionary dynamics.

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