Fossilized pollen malformations as indicators of past environmental stress and meiotic disruption: insights from modern conifers

Pollen malformations have been proposed as a paleoenvironmental stress
proxy. However, the frequency and variability of pollen malformations
under near-optimal conditions and environmental stress, as well as their
developmental origins, remain unclear. To bridge these gaps, we compared
pollen malformation frequencies and assemblages of 14 extant conifer
genera of Pinaceae and Podocarpaceae producing saccate (winged) grains
grown under near-optimal conditions. These baseline pollen yields were
compared with those produced by Pinus mugo ‘Columnaris’ cultured under an
abiotic stress—three experimentally heightened UV-B regimes proposed for
the end-Permian crisis. We additionally reviewed previous cytological
literature of abnormal microsporogenesis in conifers. Under near-optimal
conditions, malformations comprise <3% of pollen yields in 12 out
of 13 bisaccate genera and >10% of yields in the naturally
trisaccate Dacrycarpus dacrydioides. We detected no phylogenetic pattern
in malformation assemblages of the baseline comparisons. UV-B irradiated
P. mugo produced significantly higher malformation frequencies and
different assemblage compositions when compared with baseline bisaccate
lineages. We propose that pollen malformations originate during the
meiotic and tetrad stages of microsporogenesis and present a framework for
the ontogeny of different malformation types seen in the fossil record.
Malformations comprising >3% of bisaccate pollen yields can be used
as a paleoenvironmental stress proxy, but rare, naturally trisaccate
lineages are not suitable for such assessments. Furthermore, heightened
UV-B not only increases pollen malformation production, but also alters
the types of abnormalities trees produce. Different environmental stresses
may therefore leave behind distinct fingerprints in the fossil record.