Deep learning approaches to the phylogenetic placement of extinct pollen morphotypes

Abstract

The phylogenetic interpretation of pollen morphology is limited by our inability to recognize the evolutionary history embedded in pollen features. Deep learning offers tools for connecting morphology to phylogeny. Using neural networks, we developed an explicitly phylogenetic toolkit for analyzing the overall shape, internal structure, and texture of a pollen grain. Our analysis pipeline determines whether testing specimens are from unknown species based on uncertainty estimates. Features of novel specimens are passed to a multi-layer perceptron network trained to transform these features into predicted phylogenetic distances from known taxa. We used these predicted distances to place specimens in a phylogeny using Bayesian inference. We trained and evaluated our models using optical superresolution micrographs of 30 Podocarpus species. We then used trained models to place nine fossil Podocarpidites specimens within the phylogeny. In doing so, we demonstrate that the phylogenetic history encoded in pollen morphology can be recognized by neural networks and that deep-learned features can be used in phylogenetic placement. Our approach makes extinction and speciation events that would otherwise be masked by the limited taxonomic resolution of the fossil pollen record visible to palynological analysis. Significance StatementMachine learned features from deep neural networks can do more than categorize and classify biological images. We demonstrate that these features can also be used to quantify morphological differences among pollen taxa, discover novel morphotypes, and place fossil specimens on a phylogeny using Bayesian inference. Deep learning can be used to characterize and identify and morphological features with evolutionary significance. These features can then be used to infer phylogenetic distance. This approach fundamentally changes how fossil pollen morphology can be interpreted, allowing greater evolutionary inference of fossil pollen specimens. The analysis framework, however, is not specific to pollen and can be generalized to other taxa and other biological images.