The history of conifers in central Italy supports long-term persistence and adaptation of mesophilous conifer fungi in Arbutus-dominated shrublands

Highlights

• We present a mycological survey from the volcanic region of Monti della Tolfa in Italy.

• Fungi of mesic conifers adapted to live in an Arbutus-dominated thermophilous shrubland.

• Long-term persistence of fungal species is discussed based on paleobotanical data.

• Local Amanita muscaria shows a high divergence compared to European specimens.

Abstract

A mycological survey from Monti della Tolfa, a volcanic region of central Italy that originated during the Early Pleistocene and remained isolated from the mainland for at least one million years, shows that a thermophilous shrubland dominated by Arbutus unedo preserves fungal species typically associated with conifers. Pinaceae are currently absent from the study area. Palynological data from the same region show a decline of Abies and Picea around 70 ka BP and their complete disappearance during the Holocene. Pinus disappeared during the postglacial. This may have determined first the isolation of the fungal populations in relict conifer woodlands in Monti della Tolfa, and then their adaptation to the current habitat, which was favored by the presence of Arbutus unedo, a broadly receptive species towards fungal associates. Genetic sequences of an isolate of Amanita muscaria (fly agaric) from Monti della Tolfa indicate that our individual is more closely related to North American than to Eurasian populations and add new insights into the phylogeographic processes of this globally distributed species.

Introduction

Fungi are crucial organisms for the ecosystem functioning and sustainability, contributing to fundamental activities such as decomposition, nutrient cycling, and nutrient transport (Palm and Chapela, 1997). They also hold key roles in species mutualisms and interactions (Perotto et al., 2013, Angelini et al., 2015). Because of this pivotal role played by fungi in all ecosystems, fungal species composition and abundance are often used as indicators of ecosystem health and natural and human-induced environmental perturbations (Müeller et al., 2004). Despite their functional importance, fungi are not adequately considered in habitat conservation programs, drawing much less attention than animal and plant species (Heilmann-Clausen et al., 2015). This is partly due to lack of knowledge on several aspects of fungal diversity, ecology, and biogeography that still prevents the use of fungi in conservation strategies. Although millions of fungal species have been estimated to live worldwide, only a small part of them has been discovered or characterized ecologically in their natural environments (Treseder and Lennon, 2015). Little is known on both response and resilience of fungal populations and communities to long-term climate processes, as well as on their evolutionary mechanisms of adaptation to novel habitats and novel plant species interactions. Phylogenetic and biogeographical studies on fungal species, substantially based on the advances of molecular genetic data, are revealing possible distribution patterns shaped by a very long history of climate and tectonic activity (Geml et al., 2006, Geml et al., 2010, Halling et al., 2008, Wilson et al., 2017). These patterns were totally ignored until a few decades ago, when the dispersal of fungi was considered independent of the ecological and evolutionary processes that characterize plants and animals (Peay et al., 2010). The lack of data for many taxa often hampers the elaboration of biogeographical and phylogeographical reconstructions at both local and global scales (Douhan et al., 2011). The depauperate record of fungal fossils compounds the problems in calibrating the population divergence events at the base of phylogenetic and phylogeographic reconstructions, and substantially relegates the estimate of divergence time to an indirect approach (e.g. tectonics, molecular clock models, paleoecological processes).

At present, there is a general consensus on the urgent need to increase mycological surveys, in order to investigate the numbers of existing species of fungi and their distributions across habitats around the globe. Such information constitutes the baseline against which to measure changes in community composition in the different sites, in response to environmental perturbations. This is a matter of major concern if considered in the light of the ongoing anthropogenic and climate-driven environmental change, which is expected to produce harmful consequences on population stability, community structure, and biodiversity preservation. Notably, ectomycorrhizal fungi, whose communities mediate the interaction between plants and soil, prove to be very sensitive to such changes (Read et al., 2004, Tóth and Barta, 2010, Pickles et al., 2012), representing major candidates to investigate the responses and long-term adaptation strategies of fungal populations to environmental stress. In this context, paleobotany and palynology may offer a valuable tool to define the paleoenvironmental changes that often influence distribution dynamics of fungal species. Despite the high amounts of data for many regions of the world and their informative potential, paleobotanical evidence is seldom used to interpret ecological and biogeographical dynamics of fungal species.

The aim of the present paper is to contribute to the aforementioned topics by focusing on a mycological survey carried out at Allumiere (Monti della Tolfa, central Italy). We considered the vegetation history in the region and investigated the possibility that fungi typical of mesic coniferous woodland had long-term persistence and unprecedented ecological adaptation to a local Mediterranean maquis dominated by strawberry trees (Arbutus unedo).