Paleopalynologists have long assumed that most acritarchs are the resistant remains of cyst-forming marine phytoplankton. As cysts, acritarch walls are thought to be composed of algaenan, or a functionally similar complex polymer analogous to sporopollenin or dinosporin. Of course there has always been an understanding that not all acritarchs fall into this category (as algal resting stages), and, in a few cases, the phylogenetic position of some exceptions have been well documented, such as the leeches fed by Sven Manum decades ago. In recent years, Precambrian palynology has become a source of doubt with regard to the assumption that all acritarchs are algal cysts, and there are now several lines of reasoning that are eroding faith in the underlying assumptions of biological affinity of the acritarchs. Palynomorphs from non-marine earliest Neoproterozoic deposits possess vegetative walls, indicating that sporopollenin sensu lato is not a prerequisite for preservation. Others have used morphology to argue that the large acanthomorphic acritarchs characteristic of the Ediacaran System might be the resting cysts of animals, rather than algae, in part because they are outside the normal size range of Paleozoic acanthomorphs and the morphological analogs in the extant phytoplankton. This implies that the Cambro-Ordovician rise of the acritarchs as evidence of phytoplankton speciating into planktonic niches could have been a primary adaptive radiation and that the Ediacaran seas were depauperate in phytoplankton. Some large acanthomorphs found in the Cambrian Nolichucky Shale in Tennessee (USA) more resemble zooplankton egg cases or Ediacaran morphotypes than presumed marine phytoplankton cysts of the Cambrian. Ordovician acritarchs belonging to an “Opalla” complex are unlike any common phytoplankton found today, as are numerous asymmetric acritarch forms which imply a benthic, not planktonic existence. Eupoikilofusids are morphologically similar to euglenids, a group which may be basal to the chlorophytes. In combination, these morphological and organic geochemical considerations, along with new discoveries in Proterozoic and lower Palaeozoic sequences, are ushering in a new era of an expanded interpretative understanding of the biological affinities of the acritarchs that could lead to considerable revision of the early fossil record of the protoctists and subsequent understanding of the rise of ecological complexity during Neoproterozoic and Paleozoic time.