The evolution of reproduction in Ediacaran–Cambrian metazoans

The evolution of reproductive style is a fundamental aspect of metazoan life history but has not been explored holistically through the Ediacaran-Cambrian rise of metazoans. Recent molecular clock analyses based on only unequivocal metazoan fossil calibrations suggest that Porifera were present by at least 590 million years ago (Ma), all major eumetazoan clades originated in the mid-late Ediacaran, and bilaterians were probably present by the late Ediacaran. An alternating pelagic larval (potentially for dispersal) and benthic adult life cycle appears to be an ancestral feature of metazoans. A compilation of inferred reproductive styles from the fossil record reveals that the low-competition, deep-water communities of the Ediacaran Avalon macrofossil assemblage (ca. 575 to 560 Ma) had current-borne sexually produced larval with both local (non-planktotrophic, with no feeding) and more widespread (planktotrophic, with feeding) dispersal followed by vegetative growth. By ca. 560 Ma, White Sea assemblage communities in shallow settings show dense aggregations, which were often dominated by single populations of episodic sexually produced larval spatfalls. Some taxa may show potential larval philopatry. By 550 Ma, with the rise of biomineralization and colonisation of shallow marine carbonate settings, the ability to encrust hard substrates, create multiple branches via budding, and rudimentary mutual attachment of inferred clones, first appear. The dominant apparent mode of reproduction throughout the Ediacaran was therefore via current-borne sexually produced larvae followed by asexual reproduction, via either budding, fragmentation or fission. In these communities where biotic interactions were limited, this enabled colonisation of newly available soft and hard substrates followed by rapid growth. Early Cambrian communities showed increased endemism, enhanced trophic interactions and widespread macropredation. By the early Cambrian Fortunian stage (ca. 535 Ma), gonochorism (separate sexes) may have been present in priapulid worms. During Cambrian Stage 2 (ca. 532 Ma), internal fertilisation probably appeared in molluscs but widespread planktotrophy did not appear until the latest Cambrian/early Ordovician. Mutual attachment of diverse skeletal taxa became more common, particularly within reefs. Evidence for egg brooding and parental care in arthropods had appeared by the early Stage 3 (ca. 518 Ma). While reproductive styles were independently acquired, this overall pattern suggests a shift both to higher fecundity and to higher quality offspring in some groups during the Ediacaran-Cambrian Radiation, driven by increasing biotic interactions, including the rise of macropredation.