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

Abstract

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 ultraviolet-B radiation (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.

The Cenomanian/Turonian boundary in light of new developments in terrestrial palynology

“…This peculiar characteristic, though, could be the result of a taphonomic artefact rather than environmental stress; therefore, further studies are needed to validate this external trait. The few occurrences of spore dyads and tetrads were less than 1% on average and, therefore, below the baseline frequency of 3-5% above which environmental influence on spore and pollen morphology can be assumed 1,8,12,63 . They reflect the natural variation of spore and pollen morphology (e.g., 64,65 ).…”

“…Teratology is the science of malformation that occurs during the development of an organism. Spores and pollen are also known to show teratomorph morphologies, sometimes in frequencies exceeding the background values of plants grown under present-day natural conditions 1 . In palaeopalynology, teratomorphic spores and pollen have been successfully employed as a proxy for increased environmental disturbance.…”

Evidences of Teratology and Mutagenensis in Palynological Assemblages from the Middle Triassic Puesto Viejo Group, San Rafael Depocenter, Argentina. Implications of Volcanism and Regional Environmental Stress

“…Land vegetation can provide insights into ecosystem health in the fossil record. In particular, plants can uniquely indicate paleoenvironmental stresses by leaving behind structural malformations in their spores and/or pollen under conditions such as heightened radiation and chemical pollutant exposure (Visscher et al, 2004;Foster & Afonin, 2005;Bazhina et al, 2007;De Storme & Geelen, 2013;Benca et al, 2018Benca et al, , 2022Lindström et al, 2019;Looy et al, 2021). Several studies have shown that volcanism is a key factor for long-term climate change, and global warming is widely regarded to have played a contributing role in numerous past biotic crises (Sun et al, 2012;Payne & Egan, 2019;Chen & Xu, 2019).…”

“…Phytotoxic volcanic emissions and radiation stress can cause abnormalities in plants and malformed spores and pollen (sporomorphs), and tetrad formation (Mičieta & Murin, 1996;Visscher et al, 2004Visscher et al, , 2011Foster & Afonin, 2005;Yin et al, 2014;Hochuli et al, 2017;Benca et al, 2018Benca et al, , 2022Benton, 2018;Lindstrӧm et al, 2019;Grasby et al, 2020;. Numerous malformations have been shown to associate with environmental stress, but some types of morphological alterations are not suitable for environmental stress detection as they do not require stress to form, such as normally unseparated spore tetrads in some arid land lycophytes, unseparated tetrads of Classopollis pollen, or the pollen of the rare plant species that naturally produce trisaccate grains.…”

“…Malformation traits can be produced through meiotic deviations (mutations) as well as through deviations later in the sporogenesis process (tetrad/free spore stage). Both of these kinds of traits can occur within sporomorphs and some give clues into which developmental processes were disrupted" (e.g., Benca et al, 2022). Recent works demonstrated that elevated UV-B radiation increases malformations in pine pollen and that the resulting teratology exhibits the same traits as those registered in gymnosperm bisaccate pollen during the end-Permian (Benca et al, 2022, and references therein).…”