1. Introduction

The composition of species in any geographic region is determined by both evolutionary and ecological processes (Ricklefs, 1987). One metric reflecting the imprint of the evolutionary history of a biological community is the mean lineage (e.g., family or genus) age of a community (Hawkins et al., 2011), whose investigation has become an important goal of macroecology and biogeography (e.g., Hawkins et al., 2011, 2014; Lu et al., 2018; Qian et al., 2018). It is broadly accepted that species tend to retain ancestral ecological traits and distributions (i.e., phylogenetic niche conservatism; Wiens and Donoghue, 2004; Donoghue, 2008). Accordingly, regions with ancestral climatic conditions of a lineage are expected to have more taxa of the lineage with higher ages, compared to those in derived climatic conditions (Qian et al., 2013; Hawkins et al., 2014). Because most major lineages of extant species originated and diversified in tropical or tropical-like climates (e.g., angiosperms; Takhtajan, 1969), tropical climates have been considered as ancestral climatic niches for many groups of organisms. Accordingly, for those lineages that originated and diversified in tropical climates, the mean lineage age of species in a biological community is expected to be higher in regions with tropical climates, compared to regions with temperate climates (Wiens and Donoghue, 2004; Qian et al., 2013; Hawkins et al., 2014).

The age-related component of the tropical niche conservatism hypothesis has been confirmed in multiple groups of animals and plants which originated and diversified in tropical climates. For example, in animals, Stevens (2006) found that the average relative age of New World leaf-nosed bats decreases with increasing latitude while Ricklefs and Schluter (1993) found that the clades that made up bird assemblages in a tropical locality are approximately twice as old as the clades that comprised a bird assemblage in a temperate locality in North America. For flowering plants, multiple studies have documented that mean lineage age generally decreases with increasing latitude. For example, Hawkins et al. (2011, 2014) and Qian et al. (2013, 2018) found that the mean family age of angiosperm trees in both regional and local assemblages decrease with increasing latitude. Yet, these trends are not driven by latitude per se, but by climatic factors. For example, Lu et al. (2018) and Qian and Deng (2023) found that the mean genus and family ages of angiosperm species assemblage decreases with decreasing temperature and precipitation in China.

Bryophytes, including liverworts, mosses, and hornworts, are the oldest extant land plants (Ligrone et al., 2012). Unlike vascular plants, particularly angiosperms, which originated and diversified in tropical climates during the Mesozoic and early Cenozoic (Takhtajan, 1969; Wiens and Donoghue, 2004), bryophytes originated long before these eras. Although they originated about 500 million years ago (Ma) (Morris et al., 2018), belonging to a greenhouse period (635−450 Ma; Voosen, 2019; Summerhayes, 2020), during which continental glaciers were almost absent but relatively low temperatures occurred locally on the planet (National Research Council, 2011), it is thought that they likely originated and underwent their first diversification in temperate climates (Shaw et al., 2005; Wu et al., 2022). In accordance with this, the current centers of diversity of the basal lineages of bryophytes are not located in tropical regions (Wang et al., 2017; Qian et al., 2023a), suggesting that temperate, rather than tropical, climates might be an ancestral niche in bryophytes. With this circumstance, phylogenetic niche conservatism would predict that the mean lineage age of bryophytes would be higher in regions of temperate climates than those of tropical climates, a hypothesis which may be termed the 'temperate niche conservatism' hypothesis. This hypothesis remains to be rigorously tested.

Liverworts, which include ca. 7500 extant species worldwide (Laenen et al., 2018), are one of the oldest land plant lineages (Ligrone et al., 2012) and the second largest lineage of bryophytes. Qian et al. (2023a) examined geographic patterns and ecological correlates of the mean genus age of liverwort floras in China, and found that mean genus age is correlated negatively with latitude and positively with temperature and precipitation. However, they also found that regions of the greatest mean genus age are located under temperate, rather than tropical, climates in some cases. Because their study included a latitudinal gradient of only ca. 35° (approximately ranging from 18° to 53° N) that included little latitudinal gradient in tropical and boreal climates, their study does not allow drawing a robust conclusion on whether the mean genus age of liverworts is higher in temperate than in tropical regions. Because no regions of high latitudes were included in their study, their study did not address the question of whether the mean genus age of liverworts in temperate regions is higher or lower than that of boreal and arctic regions.

Here, we test the temperate niche conservatism hypothesis by investigating geographic patterns and climatic correlates of the mean genus age of liverworts in regional floras across North America. We use regional floras of liverworts in North America as our study system for several reasons. First, as noted above, liverworts likely originated and diversified in temperate climates (Morris et al., 2018), and thus are a group of appropriate organisms for testing the temperate niche conservatism hypothesis. Second, the species composition of liverworts in regional floras in North America has in general been well documented (Stotler and Crandall-Stotler, 2017; Delgadillo-Moya, 2022). Third, the latitudinal gradient of our study region covers ca. 65° (approximately ranging from 7° to 72° N) and thus almost the entire latitudinal and ecological range of liverwort communities from tropical through temperate and boreal to arctic climates, and the longitudinal gradient from eastern to western North America approximately at mid latitudes covers a water-availability gradient from moist to dry climate, a combination of which is ideal for testing climate-related ecological and evolutionary hypotheses.

In this study, we start by addressing the following two questions to assess whether liverworts in North America correspond to the temperate niche conservatism hypothesis: (1) Is the mean genus age of a liverwort flora greater in temperate than in tropical climates? (2) Is the mean genus age of a liverwort flora greater in temperate than in boreal and arctic climates? Considering that liverworts likely originated and diversified in temperate climates and thus temperate climates are ancestral niches for liverworts, following the theory of phylogenetic niche conservatism (Wiens and Donoghue, 2004; Donoghue, 2008), we predict that the mean genus age of liverwort assemblages is greater at temperate latitudes than at tropical ones (hypothesis H1). Similarly, because several basal lineages of bryophytes are species-richest in regions of temperate climates around mid-latitudes, rather than those of arctic climates at high latitudes (Shaw et al., 2005; Wu et al., 2022), we hypothesize that extremely cold climates at high latitudes are also derived niches for liverworts. Accordingly, we predict that the mean genus age of liverwort assemblages is greater in temperate climate than in boreal and arctic climates (hypothesis H2). Taken together, the mean genus ages of liverwort assemblages are expected to show a hump-shaped pattern across the latitudinal gradient from tropical to arctic regions.

However, latitude per se does not influence biotic communities, but rather the climatic factors that vary with latitude influence biotic communities. Thus, to more fully explore the underlying causes of the latitudinal pattern, and to separate the effects of precipitation- and temperature-related climatic conditions, as well as the roles of climatic extremes and seasonality, we asked two further questions: (3) Are temperature-related variables more important than precipitation-related variables, or vice versa, in shaping the geographic distribution of mean genus age of liverworts? (4) Are climate extreme variables more important than climate seasonality variables, or vice versa, in shaping the geographic distribution of mean genus age of liverworts? Temperature and precipitation both shape geographic patterns of liverworts but previous studies have shown mixed results on which of the two is a more important driver of liverwort distributions and diversity. For example, Qian and Chen (2016) found that precipitation-related variables are correlated with species richness more strongly than temperature-related variables for liverworts in China, whereas Qian et al. (2023a) found that temperature-related variables tend to be more important than precipitation-related variables in explaining the variation of the mean genus age of liverworts in China. Considering the floristic correlations between the bryophytes of eastern Asia and North America (Sharp, 1972), we predict that the relative importance of temperature- and precipitation-related variables on the mean genus age of liverworts in North America is the same as in China (i.e., temperature > precipitation; hypothesis H3).

Both climate extremes (e.g., extremely cold and extremely dry) and climate seasonality (e.g., temperature seasonality and precipitation seasonality) can affect species distribution and community structure (Qian et al., 2023b), but the relative influences of climatic extremes and climatic seasonality on biological assembly remains poorly explored. Several studies have investigated the relative influences of climatic extremes and climatic seasonality on various aspects of biological assembly of angiosperms and ferns, including species richness (Qian et al., 2022), mean lineage age (Qian et al., 2018), and phylogenetic structure (Qian et al., 2023b), and found that climatic extreme variables are a more important driver of biological assembly of angiosperms and ferns, whose ancestral niches are tropical climates, but whether this holds true for lineages whose ancestral niches are temperate climate, such as liverworts, needs to be rigorously tested. Considering that climatic extreme variables explained more variation in the mean genus age of liverworts than did climatic seasonality variables in China (Qian et al., 2023a), we predict that the finding for the Chinese liverwort floras also applies to liverwort floras in North America (i.e., climate extreme > climate seasonality; hypothesis H4).

Due to differences in paleofloras, plate tectonics, ages of mountain ranges, and climatic gradients, among others, between eastern and western North America, previous studies (e.g., Qian and Sandel, 2017, 2022) have shown that latitudinal and ecological patterns of composition and structure of biological assemblages differ substantially between eastern and western North America. Accordingly, in addition to analyzing data for North America as a whole, we also analyzed data for eastern and western North America separately. The geographic extents of these two longitudinal zones were shown in Fig. S1.

2. Materials and methods 2.1. Liverwort floras

This study included 76 geographic units defined by the World Geographical Scheme for Recording Plant Distributions (Brummitt, 2001) at the level 3 in North America (Fig. S1). These geographic units have been commonly used to document species distributions for studies on macroecology and biogeography (e.g., Zhang et al., 2018; Sandel et al., 2020). Species lists of native liverworts in these geographic units were obtained from Collart et al. (2021), and additional sources (e.g., Stotler and Crandall-Stotler, 2017). Botanical nomenclature of liverworts was standardized according to Bryophyte Nomenclator (Brinda and Atwood, 2023), using the package U.Taxonstand (Zhang and Qian, 2023). Infraspecific taxa were combined with their respective species. As a result, a total of 1291 species of liverworts in 190 genera were included in this study.

2.2. Mean genus age

We obtained data for the genus ages of liverworts from Laenen et al. (2014). Laenen et al. (2014) estimated ages for each genus based on three increasingly conservative approaches according to the fossil record and phylogenetic estimates. We used the average value of the three estimated ages of each genus. Twenty-seven of the 190 genera in our study were absent from Laenen et al. (2014). We estimated ages of these genera based on their sister or closely related genera (Table S1), for which data of genus ages were available in Laenen et al. (2014).

We calculated two metrics of mean genus age (MGA) for each of the 76 geographic units as in Qian et al. (2023a): one metric was based on the presence or absence of each genus in each geographic unit (i.e., MGA based on genus incidence), and the other based on species richness of each genus in each geographic unit (i.e., MGA based on genus abundance, or richness-weighted MGA), using the following formula: MGA = Σ(G_i × S_i)/Σ(S_i), where i = 1, 2, 3, …, n, G_i = age of a genus i, and S_i = the number of species in the genus i (Lu et al., 2018; Qian et al., 2023a). For both MGA metrics, we also calculated standardized effect size (ses) for each geographic unit based on a null model, as follows: X_ses = (X_obs − X_null)/sd(X_null), where X_ses represents standardized effect size for X (i.e., one of the metrics under consideration), X_obs is the observed X of an assemblage, X_null is the expected (i.e., average) X of the randomized assemblages, and sd(X_null) is the standard deviation of X for the randomized assemblages (N = 999). When calculating X_ses based on data of species richness per genus, to generate a randomized assemblage, we randomized genus ages and assigned all species the age of the genus they belong to. This approach, or a similar one, has been used in multiple studies (e.g., Zhao et al., 2018; Qian and Deng, 2023; Qian et al., 2023a). A negative value of standardized effect size indicates that an observed value was lower than the average expected value, whereas a positive value indicates that an observed value was higher than the average expected value.

2.3. Climatic data

The following climatic variables represent annual averages, seasonality, and climatically limiting factors: mean annual temperature (T_mean), minimum temperature of the coldest month (T_min), temperature seasonality (T_seas), annual precipitation (P_mean), precipitation during the driest month (P_min), and precipitation seasonality (P_seas). These climatic variables, which have been commonly related to measures of biological communities (e.g., Qian and Sandel, 2017; Khine et al., 2019), are relevant to the questions addressed in this study. Temperature-related variables included T_mean, T_min, and T_seas, and precipitation-related variables included P_mean, P_min, and P_seas. Climate extreme variables included T_min and P_min, and climate seasonality variables included T_seas and P_seas. We obtained data for these climatic variables at the 30-arc-second resolution from the CHELSA climate database (https://chelsa-climate.org/bioclim; version 2.1) (Karger et al., 2017), and calculated the mean value of each of the climate variables for each of the 76 geographic units. We considered a region under tropical climate if its mean annual temperature being > 20 ℃, temperate climate if its mean annual temperature being ≤ 20 ℃ and ≥ 5 ℃, or boreal-arctic climate if its mean annual temperature being < 5 ℃ (Ricklefs, 2008).

2.4. Data analysis

We used t-test to determine statistical significance in difference in mean genus age of liverwort assemblages between temperate and either tropical or boreal-arctic climates. We conducted correlation and regression analyses to assess the relationships between genus-age metrics of liverworts and environmental variables. We used Spearman's correlation coefficient (r_s), unless stated otherwise, and considered it to be strong for |r_s| > 0.66, moderate for 0.66 ≥ |r_s| > 0.33, and weak for |r_s| ≤ 0.33 (Qian et al., 2019). We used spatial simultaneous autoregressive error models to examine the relationships between genus-age metrics and climatic variables. To determine whether temperature-related variables or precipitation-related variables have a stronger influence on each of the genus-age metrics, we conducted a set of partial regressions (Legendre and Legendre, 2012) to partition the explained variation into three portions: variation explained independently by temperature-related variables, variation explained independently by precipitation-related variables, and variation explained jointly by the temperature- and precipitation-related variables. Similarly, to determine whether climate extreme variables or climate seasonality variables have a stronger influence on each of the genus-age metrics, we conducted another set of partial regressions to partition the explained variation into three portions: variation explained independently by climate extreme variables, variation explained independently by climate seasonality variables, and variation explained jointly by climate extreme and seasonality variables. Each regression was a second-order polynomial model. We used the packages SYSTAT (Wilkinson et al., 1992) and Spatial Analysis in Macroecology (www.ecoevol.ufg.br/sam/; Rangel et al., 2010) for statistical analyses.

The analyses of this study emphasized on MGA based on genus abundance in each geographic unit (i.e., richness-weighted MGA), because species composition is a better representation of biological composition and previous studies on mean lineage age also focused on species-weighted mean lineage age (e.g., Hawkins et al., 2014; Zhao et al., 2018). However, we also conducted analyses on MGA based on genus incidence (i.e., presence or absence). In most cases, we reported the results derived from the data of MGA based on genus abundance in the main text and reported the results derived from the data of MGA based on genus incidence in the supplementary materials.

3. Results

Geographic patterns of MGA based on genus incidence differed greatly from those based on genus abundance, and this held regardless of whether MGA or MGA_ses was considered (compare Fig. 1a, c with Fig. 1b, d). When MGA based on genus incidence was considered, both MGA and MGA_ses generally increased with increasing latitude regardless of whether North America was considered as a whole or eastern and western North America were considered separately (Figs. 1a, c and S2). In contrast, when MGA based on genus abundance was considered, both MGA and MGA_ses generally decreased with increasing latitude in both eastern and western North America (Figs. 1b, d and S3). However, for North America as a whole and for eastern North America, both MGA and MGA_ses showed a hump-shaped pattern across the latitudinal gradients, regardless of whether MGA based on genus incidence or MGA based on genus abundance was considered (Figs. 2 and S2). While geographic patterns of MGA based on genus incidence differed greatly from those based on genus abundance, geographic patterns of MGA were similar to those of MGA_ses (compare Fig. 1a with 1c, and Fig. 1b with 1d).

When MGA and MGA_ses based on genus incidence were considered, they both were significantly greater in temperate climate than in tropical climate (P < 0.05), but did not differ between temperate and boreal-arctic climates (P > 0.50) (Table S2). When MGA and MGA_ses based on genus abundance were considered, MGA in temperate climate was marginally significantly greater than MGA in tropical climate (P = 0.057), and was significantly greater than MGA in boreal-arctic climate (P < 0.05; Table 1); MGA_ses in temperate climate was significantly greater than MGA_ses in both tropical and boreal-arctic climates (P < 0.05 in both cases; Table 1).

Due to the strong and negative correlation between latitude and mean annual temperature (r_s = -0.979, N = 76), the relationships of MGA and MGA_ses with mean annual temperature mirrored those with latitude (compare Fig. S3 with Fig. 2, Fig. S3 with Fig. S4). In North America as a whole and among the six climatic variables examined in this study, precipitation during the driest month (P_min) was most strongly associated with MGA and MGA_ses (Table S3). When eastern and western North America were considered separately, for each of the six climatic variables, the relationship of MGA or MGA_ses with the climatic variable was much stronger for eastern North America than for western North America, except for the relationship between MGA_ses and P_mean (Table S3), and the explained variation varied much more greatly among the six climatic variables for eastern North America than for western North America (Table S3). In eastern North America, minimum temperature of the coldest month (T_min) was most strongly associated with MGA and MGA_ses (Table S3).

In North America as a whole, the six climatic variables together explained 67.9% and 69.6% of the variation in MGA and MGA_ses, respectively. In either case, nearly all variation was independently explained either by the temperature-related variables or by the precipitation-related variables, with the latter explaining more variation than the former (Fig. 4). When eastern and western North America were considered separately, the six climatic variables explained much more variation in either genus age metric in eastern North America, compared to western North America (73.4% versus 42.9% for MGA; 77.9% versus 46.0% for MGA_ses). In eastern North America, the amount of variation explained jointly by the temperature- and precipitation-related variables was greater than that explained either independently by the temperature-related variables or independently by precipitation-related variables, and the amount of variation explained independently by the temperature-related variables was greater than that explained independently by the precipitation-related variables, regardless of whether MGA or MGA_ses was considered (Fig. 4). In western North America, the temperature-related variables independently explained slightly more variation in MGA and slightly less variation in MGA_ses, compared to the precipitation-related variables (Fig. 4). The climatic extreme variables independently explained more variation in both MGA and MGA_ses, compared to the variation independently explained by the climatic seasonality variables, regardless of whether North America was considered as a whole or eastern and western North America were considered separately (Fig. 5).

4. Discussion

In this study, we have, for the first time, documented the geographic and ecological patterns of the mean genus age (MGA) of liverworts across a nearly full latitudinal gradient ranging from tropical Panama to arctic Canada and Alaska. Overall, we found a hump-shaped latitudinal pattern of MGA, with the highest ages at temperate latitudes, in accordance with our hypotheses H1 and H2. This agrees with the temperate niche conservatism hypothesis, according to which liverworts originated under climatic conditions akin to those today found at temperate latitudes, so that the oldest genera are found there, while younger genera have partly adapted to novel climatic conditions (both tropical and boreal/arctic). This general pattern is in accordance with previous suggestions that liverworts originated and diversified under temperate climate conditions (Shaw et al., 2005; Wu et al., 2022, Qian et al., 2023a; K. Maul, M. Kessler et al. unpubl. data). Indeed, today the contemporary centers of diversity for the basal liverwort lineages are found in temperate regions (Wang et al., 2017; Qian et al., 2023a). However, our finding is inconsistent with the finding of a study on the mean phylogenetic distance of liverworts in elevational belts across an elevational gradient in the central Himalaya (H. Qian, unpubl. data), possibly because biological patterns may differ between latitudinal and elevational gradients (Qian and Ricklefs, 2016), and because of the unique evolutional history of the flora of the central Himalaya (Qian et al., 2019).

This overall pattern becomes more complex once we focus more closely. Most importantly, the hump-shaped latitudinal pattern of MGA of liverworts is driven by eastern North America, whereas the western side of the continent shows a strikingly different pattern, with a monotonic decrease in MGA, so that liverwort genera are on average oldest at subtropical latitudes (the western side defined in this study does not reach the tropics). Previous studies found that geographic patterns of angiosperm assemblages also differ substantially between eastern and western North America. For example, the relationship between latitude and standardized phylogenetic diversity in angiosperms is negative in eastern North America and positive in the West (Qian and Sandel, 2017). These differences between the East and the West are likely due to the different climatic conditions. The East is generally humid, with temperature and precipitation both decreasing with increasing latitude (r_s = -0.96 and -0.82, respectively, in our dataset). In contrast, the West is mostly quite arid and has an 'atypical' precipitation gradient so that while temperature decreases with increasing latitude (r_s = -0.96), precipitation decreases only weakly (-0.10) or even increases when only western North America north of Mexico is considered (r_s = 0.18). This precipitation pattern is driven by the combination of the rain-shadow effect of the Rocky Mountains, which block rainfall coming via the eastern trade winds, and the influence of cold sea currents off the western coast, which create desertic conditions in the south whereas the coastal area of the Pacific Northwest is under the track of the jet stream and receives abundant precipitation from the west. As a result, the latter area supports the development of temperate rain forests, which support a rich flora of bryophytes (Wu et al., 2022). These differences between the eastern and western parts of the continent show that the latitudinal pattern of MGA in liverworts is not driven by latitude per se, but is also strongly influenced by precipitation. In fact, we found that, contrary to our hypothesis H3, precipitation-related climatic variables had the strongest relationship with MGA when looking at the whole study region. This has also previously been found for liverwort species richness in China (Qian and Chen, 2016).

The strong influence of precipitation on the richness and MGA of liverworts can readily be related to their physiology. As a group of poikilohydric plants, liverworts lack vascular tissue and outer cuticle, and the water content of liverworts is directly regulated by ambient humidity so that most liverwort species rely on atmospheric precipitations for water uptake (Patiño and Vanderpoorten, 2018). Consequently, physiological activity of liverworts is restricted to the time when water is available, and the metabolism of liverworts suspends when water is lacking (Gignac, 2001). Furthermore, the process of sexual reproduction and spore germination of liverworts depend on water, so that water availability is expected to be essential for the dispersal of liverworts, which is primarily driven by spores (Proctor et al., 2007; Aranda et al., 2014).

However, the predominance of precipitation-related variables only holds overall and for the West. When focusing on the eastern part of the continent, temperature-related climatic variables explained more variation in MGA than did precipitation-related climatic variables. In this region, MGA peaks at latitudes between 30° and 40° N, which correspond to mean annual temperature of 10 ℃–20 ℃ (Fig. 3), representing temperate climate (Ricklefs, 2010). Interestingly, the standardized effect size of the MGA of liverworts in China also peaks at latitudes between 30° and 40° N (Qian et al., 2023a), with mean annual temperature also ranging approximately from 10 ℃ to 20 ℃. However, because the latitudinal gradient in their study is only 35° long, which is relatively short, the hump-shaped pattern of the MGA of liverworts is not conspicuous in their study. In contrast, the latitudinal gradient in our study is long (covering 65°), and shows conspicuous hump-shaped patterns of the MGA of liverworts across latitude (Fig. S3) and temperature (Fig. 3). A predominance of temperature- over precipitation-related variables in determining the phylogenetic structure of regional floras has also been found in ferns and angiosperms (Qian et al., 2023b).

The shifts in the weights of temperature and precipitation between regions and taxonomic groups in determining the diversity and structure of plant communities likely have two reasons. First, on average bryophytes and ferns are likely more dependent on water availability than angiosperms, increasing the ecological relevance of precipitation. Second, the range of climatic variables represented in a certain geographic region will be crucial. Thus, we propose that the diminished role of precipitation-related variables, relative to the role of temperature-related variables, found in eastern North America in this study is because this region mostly has a humid climate, so that the range of precipitation values does not reach the arid conditions that are limiting for many liverwort taxa. This interpretation is supported by the striking differences of the patterns recovered when considering only the presence or absence of a genus against weighting the genera by species richness provide important information. When looking at the presence or absence of each genus in a region, we find that both MGA and MGA_ses are largest in temperate latitudes and are smaller in tropical latitudes than in boreal-arctic latitudes (Fig. S2), suggesting that old genera are overrepresented at temperate latitudes whereas young genera are overrepresented in the tropics and to a lesser degree in arctic regions. When weighting genera by the number of species, we find an overrepresentation of old genera in the East (Fig. 1b). This shows that older genera, although present, tend to be less species rich than younger genera in the West. Considering that the West is generally drier than the East, we propose that old genera appear to favor humid environmental conditions and probably only occur locally with few species in humid habitat pockets in the West, whereas they dominate the more humid habitats in the East. That this is not found for temperature has to do with the fact that humid microhabitats can readily be formed even in arid regions, whereas temperature is less easily modified locally.

Looking in more detail at the role of climatic variables, we found that climate extremes explained more variation in MGA of liverworts than did climate seasonality variables, supporting our hypothesis H4. This finding is consistent with that of Qian et al. (2023a) for liverworts in China, of Qian et al. (2018) for the mean family age of angiosperm trees in the eastern United States, and of Li et al. (2022) for the mean family age of angiosperms in eastern Himalaya. Moreover, several studies on other community metrics (e.g., phylogenetic relatedness) of assemblages of vascular plants also found that climate extreme variables are more important than climate seasonality variables in biological community assembly (Li et al., 2022; Qian et al., 2022). This consistence among different studies on different groups of plants suggests that the conclusion that climate extreme variables are more important drivers of MGA and other metrics of plant (including liverwort) communities, compared to climate seasonality variables, is robust. The biological explanation of this probably is that it is easier and more important for organisms to adapt to regularly recurring climatic conditions, such as annual cycles, than to extreme conditions that only appear occasionally.

Finally, comparing the patterns of MGA with those of taxonomic diversity, we find that genus and species richness in liverworts decrease monotonically with increasing latitude in North America (Fig. S5). This is consistent with the pattern of decreasing richness with increasing latitude that has been commonly found in most groups of organisms (e.g., angiosperms, ferns, and many animal lineages) (Rosenzweig, 1995; Khine et al., 2019; Qian et al., 2019, 2023b), but contrasts with the hump-shaped latitudinal gradient of MGA in liverworts. The pattern of increasing richness but decreasing MGA towards the tropics in liverworts may be explained as a result of a more recent origin of tropical diversity in combination with significantly higher net diversification rates in some tropical liverwort lineages, notably Lejeuneaceae, compared to extra-tropical genera (Laenen et al., 2018; K. Maul, M. Kessler et al. unpubl. data).

Concluding, we found that older genera of liverworts tend to be concentrated in regions of high precipitation and intermediate temperatures in the range of 10 ℃–20 ℃, presumably corresponding to the ancestral climatic niche of extant liverwort lineages (Shaw et al., 2005; Wu et al., 2022; K. Maul, M. Kessler et al. unpubl. data). From this ancestral niche, liverworts have adapted to and diversified into more arid, colder, and hotter regions, with high diversification rates in the humid tropics (Laenen et al., 2018, K. Maul, M. Kessler et al. unpubl. data). Overall, this is consistent with the notion of phylogenetic niche conservatism, of which the case of tropical niche conservatism is best known (Wiens and Donoghue, 2004). We started this study by proposing that liverworts represent a case of temperate niche conservatism, but considering the importance of humidity, liverworts may best be characterized as showing humid-temperate niche conservatism. Geographic and ecological patterns of the mean genus age of liverworts observed in this study provide support for the temperate niche conservatism hypothesis, which is proposed to explain distributions of taxa in lineages originated and diversified in temperate climates.

Acknowledgements

We thank two anonymous reviewers for their helpful comments.

Data availability statement

This study used liverwort species distribution data available from the Figshare Repository at https://doi.org/10.6084/m9.figshare.22587199, and climate data available at the CHELSA climate database (https://chelsa-climate.org/bioclim).

CRediT authorship contribution statement

Hong Qian: Writing – review & editing, Writing – original draft, Investigation, Data curation, Conceptualization. Jian Wang: Data curation. Shenhua Qian: Writing – review & editing, Formal analysis. Michael Kessler: Writing – review & editing, Writing – original draft.

Declaration of competing interest

The authors have no competing interest to declare.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.pld.2024.07.002.