Early evolution of life cycles in embryophytes: A focus on the fossil evidence of gametophyte/sporophyte size and morphological complexity

Abstract

Embryophytes (land plants) are distinguished from their green algal ancestors by diplobiontic life cycles, that is, alternation of multicellular gametophytic and sporophytic generations. The bryophyte sporophyte is small and matrotrophic on the dominant gametophyte; extant vascular plants have an independent, dominant sporophyte and a reduced gametophyte. The elaboration of the diplobiontic life cycle in embryophytes has been thoroughly discussed within the context of the Antithetic and the Homologous Theories. The Antithetic Theory proposes a green algal ancestor with a gametophyte-dominant haplobiontic life cycle. The Homologous Theory suggests a green algal ancestor with alternation of isomorphic generations. The shifts that led from haplobiontic to diplobiontic life cycles and from gametophytic to sporophytic dominance are most probably related with terrestrial habitats. Cladistic studies strongly support the Antithetic Theory in repeatedly identifying charophycean green algae as the closest relatives of land plants. In recent years, exceptionally well-preserved axial gametophytes have been described from the Rhynie chert (Lower Devonian, 410 Ma), and the complete life cycle of several Rhynie chert plants has been reconstructed. All show an alternation of more or less isomorphic generations, which is currently accepted as the plesiomorphic condition among all early polysporangiophytes, including basal tracheophytes. Here we review the existing evidence for early embryophyte gametophytes. We also discuss some recently discovered plants preserved as compression fossils and interpreted as gametophytes. All the fossil evidence supports the Antithetic Theory and indicates that the gametophytic generation/sporophytic generation size and complexity ratios show a gradual decrease along the land plant phylogenetic tree.

Sex and the Single Gametophyte: Revising the Homosporous Vascular Plant Life Cycle in Light of Contemporary Research

“…Each of these phases is multicellular, but they vary (among major lineages) in duration and size (see figure 2 in Qiu et al 2012, figure 16 in Gerrienne andGonez 2011). The exact relationships of the major bryophyte lineages (mosses, liverworts, and hornworts) to one another and to vascular plants are still unresolved (Wickett et al 2014), but all three bryophyte lineages feature a long-lived gametophyte phase and an ephemeral sporophyte phase that is nutritionally dependent on the more prominent gametophyte.…”

“…In this system, ferns and lycophytes are distinguished from all other plants by a life cycle featuring fully independent gametophyte and sporophyte phases (also referred to as generations), with the sporophyte being dominant (i.e., the most obvious and generally the longest lived). Recent classifications based on fossil evidence and molecular phylogenetic studies have only reinforced the conclusion that changes in life cycles have been a major correlate and driver of evolution in plants (Gerrienne andGonez 2011, Qiu et al 2012).…”

Evolution of the life cycle in land plants

“…2). At an early stage in land colonization by plants, the haploid phase did experience some degree of elaboration, to the point that several extinct stem relatives of vascular plants possessed well developed and complex diploid and haploid phases (Remy et al, 1993; Kenrick, 1994, 2000; Taylor et al, 2005; Gerrienne & Gonez, 2011), perhaps because the environment was more favorable for plants with a haploid phase‐dominant life cycle. Below we will discuss several aspects of life cycle evolution that underlie major transitions in land plant evolution.…”

Estimating pairwise relatedness between individuals with different levels of ploidy

“…), polyhaploids (Behnke ; Hermsen et al . ) and gametophytes vs. sporophytes (Shaw & Beer ; Gerrienne & Gonez ). In this study, five relatedness coefficient estimators are extended to various mixtures of ploidy.…”

“…). The ploidy of gametophytes in some organisms such as lichens and mosses are also halved relative to the diploid state (Shaw & Beer ; Gerrienne & Gonez ).…”