INTRODUCTION

Addressing the impact of global warming on plants requires an understanding of multiple traits across plant life stages, not only within but also across generations. Warming, as associated with climate change, has a strong effect on phenotypic traits throughout a plant’s life cycle. Warmer temperatures generally lead to increased biomass and vegetative growth (Debouk, de Bello, & Sebastià, 2015; King, Pregitzer, & Zak, 1999; Lin, Xia, & Wan, 2010; Walker et al., 2006), reduced flower numbers and seed production (Hedhly, Hormaza, & Herrero, 2009; Liu, Mu, Niklas, Li, & Sun, 2012), increased mortality at both seedling and adult stages (Allen et al., 2010; Hovenden et al., 2008; Milbau, Vandeplas, Kockelbergh, & Nijs, 2017), delays and decreases in seedling emergence (Cochrane, Hoyle, Yates, Wood, & Nicotra, 2015), and potentially can lead to local extirpation of the species (Panetta, Stanton, & Harte, 2018). Phenology, the timing of biological events – e.g. bud burst, flowering, seed set, and senescence – is thought to be the characteristic that is most sensitive to warming and hence, most observations of responses to climate change have focused on shifts in phenology (Arft et al., 1999; Cadman, Toorop, Hilhorst, & Finch-Savage, 2006; Cleland, Chuine, Menzel, Mooney, & Schwartz, 2007; Farnsworth, Nunez-Farfan, Careaga, & Bazzaz, 1995; Jin et al., 2011; Körner & Basler, 2010; Menzel et al., 2006; Moore & Lauenroth, 2017; Munson & Sher, 2015; Peñuelas & Filella, 2001; Rathcke & Lacey, 1985; Root et al., 2003; Sherry et al., 2007; Walther et al., 2002).
Warming responses of vegetative growth, reproductive output and phenological traits (including senescence) should not, however, be viewed in isolation (Hoffmann & Sgrò, 2011; Leblans et al., 2017; Merilä & Hendry, 2014; Nicotra et al., 2010). Rather, variation in trait values and timing of phenological events determines subsequent interactions of the individual with the environment and because of this co-dependence, the responses to environmental change are likely to be quite complex. For example, germination timing (spring versus autumn) determines the seasonal conditions and duration of seedling exposure as well as the conditions in which subsequent life stages occur. Accordingly, germination timing determines conditions at flowering time, reproductive period and lifespan in annuals (Donohue, 2009; Lu, Tan, Baskin, & Baskin, 2016). Time to flowering, likewise, could determine the season of seed maturity with implications for germination timing, and the germination timing could in turn determine whether the offspring will become annual or biennial (Galloway, 2005; Galloway & Etterson, 2007). Thus, a shift in the timing of one phenological event can have cascading effects for the subsequent life events. However, these shifts do not necessarily all occur in concert, for example, early flowering in response to warming is not always followed by a change in timing of cessation of flowering and thus may result in the expansion or contraction of the flowering period (CaraDonna, Iler, & Inouye, 2014).
Warming effects may also be highly species- or even population-specific. For example, prairie species that have early-flowering (spring to mid-summer) start to flower even earlier, and conversely, late-flowering species (mid-summer to autumn), delay their flowering when exposed to warming treatments (Dunnell & Travers, 2011; Sherry et al., 2007). In the sub-arctic herb Cerastium fontanum, plants from warmer microsites (populations) flower earlier than those from colder microsites but when grown in much warmer common gardens, plants from warmer microsites start to flower later than plants originating from colder microsites (Valdés, Marteinsdóttir, & Ehrlén, 2019). In the alpine herb Aciphylla glacialis, seedlings growing under an open top chamber exhibit higher mortality (but surviving individuals grow faster) than those under ambient conditions (Geange, Holloway-Phillips, Briceño, & Nicotra, 2020), regardless of the population source (Briceño, Harris-Pascal, Nicotra, Williams, & Ball, 2014). Species response to warming may also be dictated by functional traits. Between geographically co-occurring species, the seedlings of fast-growingBanksia coccinea, characterized by higher SLA (specific leaf area) and leaf growth rate, can maintain growth at high temperatures better than its slow-growing congeneric B. baxteri (Cochrane, Hoyle, et al., 2015). Within a plant’s life cycle, response to elevated temperatures can also be trait-specific. For example, inArabidopsis thaliana warming advances flowering time, accelerates vegetative development and fruit production but not plant mortality (Springate & Kover, 2014). So far, the studies on plant responses to climate change often focus only on particular suites of traits (e.g. leaf traits or flowering phenology) and only at a certain life stage (mostly adult reproductive), which may lead to incomplete assessments and failure to predict the cascading effects of warming on species’ persistence, and thus community composition and ecosystem functions and services.
While research on the adaptive capacity of plants under future climate is increasing, we still lack understanding of plant plasticity and their capacity to evolve when challenged by new environmental conditions, especially for germination and the seedling stage (Parmesan & Hanley, 2015). Studies across ontogeny that span whole life events, and multiple generations, are also lacking. Maternal conditions may have carry-over effects across generations and could determine the life history of the progeny (Donohue, 1998; Donohue, 2009). When these maternal effects increase offspring fitness, this trans-generational plasticity may be adaptive (Galloway, 2001a, 2001b, 2005; Galloway & Etterson, 2007; Herman & Sultan, 2011). For example, warmer temperatures during seed development generally reduce the degree of primary seed dormancy (Bernareggi, Carbognani, Mondoni, & Petraglia, 2016; Gutterman, 2000; Hoyle, Steadman, Daws, & Adkins, 2008; Huang, Footitt, Tang, & Finch-Savage, 2018), enabling individuals to start growing and to reach reproductive stage earlier in the season and thus have a longer duration for seed production and potentially produce more seeds (Donohue, de Casas, Burghardt, Kovach, & Willis, 2010; Roach & Wulff, 1987). Climate induced variation in seed dormancy status, in turn, may play shift timing of germination or variance therein, providing a buffer against disturbances that may be a bet-hedging strategy. Changes in dormancy may also affect seedling growth rate and establishment (Satyanti, Guja, & Nicotra, 2019), or physiological traits such as water use efficiency, reproductive phenology and senescence (Kimball, Angert, Huxman, & Venable, 2010, 2011). Understanding the extent to which germination strategy, particularly the degree of dormancy and how it is lost over time, could change with warming and whether maternal temperature interacts with offspring germination requirements to affect germination success will be valuable for predicting species persistence in the face of a changing climate.
Alpine regions are recognized as one of the most vulnerable ecosystems under warming climates – impacts are forecast to be pronounced and detectable earlier than in other biomes (Grabherr, Gottfried, & Pauli, 2010). Alpine plants that are adapted to low temperature and a short growing season are particularly responsive to warming (Anadon-Rosell et al., 2014; Arft et al., 1999; Bjorkman, Elmendorf, Beamish, Vellend, & Henry, 2015; Cao et al., 2016; Geange et al., 2017; Geange et al., 2020; Kudernatsch, Fischer, Bernhardt-Römermann, & Abs, 2008; Kudo & Suzuki, 2003; Oberbauer et al., 2013). Perhaps paradoxically, seeds of alpine plants generally require relatively high soil temperature to trigger germination (Hoyle et al., 2013; Schütz, 2000; Schütz & Milberg, 1997) and hence, warming could have a positive effect on recruitment via seed. In strongly seasonal and unpredictable environments, plants often evolve specific seed dormancy that leads to divergence in germination strategy (Hoyle et al., 2015; Satyanti et al., 2019; Willis et al., 2014). Variation of germination strategy across alpine species is common (Hoyle et al., 2015; Körner, 2003; Satyanti, 2018), but more strikingly, intraspecific variation in germination strategy with environment and elevation is also documented (e.g. Hoyle et al., 2015; Satyanti et al., 2019; Vidigal et al., 2016; Wagner & Simons, 2009). Such variation in germination strategy may help to facilitate the regeneration and survival of plants in short growing seasons, and highly variable environments, as reported from (Satyanti et al., 2019).
Oreomyrrhis eriopoda (Apiaceae) is a native rosette-forming herb from the Australian Alps that exhibits has four germination strategies: immediate, staggered, postponed, and postponed-deep (Satyanti et al., 2019). Populations with an immediate strategy produce non-dormant seed and thus “autumn seedlings”. Populations that produce dormant seeds (postponed strategy) produce “spring seedlings”. Populations categorised as postponed-deep germinate (usually in spring) after exposure to multiple cycles of winter conditions. Populations that exhibit the staggered strategy produce both non-dormant and postponed seeds in the same accession and thus both “autumn” and “spring seedlings” occur (e.g. Hoyle et al., 2015; Satyanti et al., 2019). The among-population variation in germination strategy in O. eriopodaleads to substantial differentiation of seedling growth among and within populations (in staggered populations autumn seedlings grow faster than spring seedlings) (Satyanti et al., 2019).
So far, we know little about the extent of intraspecific germination strategy variation in plant responses to warming. Particularly, to what extent plants are able to increase growth rate and to adjust phenology to maximise reproductive capacity and fitness. Using O. eriopoda , we aim to understand the effect of warming across all life stages (vegetative growth, reproductive output, phenology and the germination traits of the seed produced), and to explore whether populations of different germination strategies show variation in those warming responses in the current and subsequent generation. We hypothesised that: (i) Warming would interact with germination strategies and overall would enhance growth at the cost of flower and fruit production, and likely with an increase in plant mortality; (ii) Plant responses to soil temperature would depend on germination strategy; (iii) Germination strategy of the offspring will be affected by warming of the maternal environment.