Current and historical factors drive variation of reproductive traits in unisexual mosses in Europe: A case study

Abstract

Unisexual bryophytes provide excellent models to study the mechanisms that regulate the frequency of sexual versus asexual reproduction in plants, and their ecological and evolutionary implications. Here, we determined sex expression, phenotypic sex ratio, and individual shoot traits in 242 populations of the cosmopolitan moss Pseudoscleropodium purum spanning its whole distributional range. We tested whether niche differentiation, sex-specific differences in shoot size, and biogeographical history explained the spatial variation of reproductive traits. We observed high levels of sex expression and predominantly female-biased populations, although both traits showed high intraspecific variation among populations. Sex expression and sex ratio were partly explained by current macroscale environmental variation, with male shoots being less frequent at the higher end of the environmental gradients defined by the current distribution of the species. Female bias in population sex ratio was significantly lower in areas recolonized after the last glacial maximum (recent populations) than in glacial refugia (long-term persistent populations). We demonstrated that reproductive trait variation in perennial unisexual mosses is partially driven by macroscale and historical environmental variation. Based on our results, we hypothesize that sexual dimorphism in environmental tolerance and vegetative growth contribute to sex ratio bias over time, constraining the chances of sexual reproduction, especially in long-term persistent populations. Further studies combining genetic analyses and population monitoring should improve our understanding of the implications of the intraspecific variation in the frequency of sexual versus asexual reproduction in bryophyte population fitness and eco-evolutionary dynamics.

Life-history characteristics and historical factors are important to explain regional variation in reproductive traits and genetic diversity in perennial mosses

“…This suggests that fertilization is, to some degree, mate limited in both species and limited by male mates in D. turgescens . Mate-limited reproduction has previously been suggested based on negative correlations between strong female sex ratio bias and low sporophyte frequency (but see Boquete et al , 2023 ) and confirmed experimentally in two mosses ( Bisang et al , 2004 ).…”

“… Chopra and Bathla, 1983 ; Rydgren and Økland, 2002 ), and geographical variation in sex phenotypes and sex expression have been demonstrated repeatedly in different plant groups ( Benassi et al , 2011 ; Yakimowski and Barrett, 2014 ; Blackstock, 2015 ; Pereira et al , 2016 ). Sex expression rates differed between different microenvironments in the desert moss Syntrichia caninervis ( Baughman et al , 2017 ; Ekwealor et al , 2022 ) and varied across Europe along macroscale environmental gradients in the perennial pleurocarpous moss Pseudoscleropodium purum ( Boquete et al , 2023 ). However, little is known about environmental effects on genotypic sexes in bryophytes (Bisang et al , 2015 , 2020 ).…”

“…In situations with restricted sexual recruitment, a sex ratio bias can remain over long periods ( Barrett, 2015 ; Hedenäs et al , 2021 ). For several bryophyte species, the time available for colonization after the Last Glacial Maximum was suggested to contribute to skewed population sex ratios ( Alonso-García et al , 2020 ; Bisang et al , 2020 ; Boquete et al , 2023 ). In vascular herbaceous plants, clonality was associated with female-biased sex ratios ( Charpentier, 2002 ; Barrett, 2015 ).…”

“…Different historical factors, such as founder events, glaciation history, climate fluctuation or immigration routes, have indeed been shown to influence regional variation in reproductive traits at various scales (e.g. Alsos et al , 2005 ; Field et al , 2013 b ; Hedenäs, 2017 ; Carter, 2021 ; Boquete et al , 2023 ). Finally, such differences are likely to be reflected in sex-related patterns of genetic diversity and genetic structure ( Dering et al , 2016 ; Zhai et al , 2016 ).…”