Evolution of life cycles and reproductive traits: Insights from the brown algae

Abstract

A vast diversity of types of life cycles exists in nature, and several theories have been advanced to explain how this diversity has evolved and how each type of life cycle is retained over evolutionary time. Here, we exploited the diversity of life cycles and reproductive traits of the brown algae (Phaeophyceae) to test several hypotheses on the evolution of life cycles. We investigated the evolutionary dynamics of four life‐history traits: life cycle, sexual system, level of gamete dimorphism and gamete parthenogenetic capacity. We assigned states to up to 77 representative species of the taxonomic diversity of the brown algal group, in a multi‐gene phylogeny. We used maximum likelihood and Bayesian analyses of correlated evolution, while taking the phylogeny into account, to test for correlations between traits and to investigate the chronological sequence of trait acquisition. Our analyses are consistent with the prediction that diploid growth evolves when sexual reproduction is preferred over asexual reproduction, possibly because it allows the complementation of deleterious mutations. We also found that haploid sex determination is ancestral in relation to diploid sex determination. However, our results could not address whether increased zygotic and diploid growth are associated with increased sexual dimorphism. Our analyses suggest that in the brown algae, isogamous species evolved from anisogamous ancestors, contrary to the commonly reported pattern where evolution proceeds from isogamy to anisogamy.

Selection drives convergent gene expression changes during transitions to co-sexuality in haploid sexual systems

“…In these brown algae, sexuality is expressed in the haploid generation, with male and female gametes produced either by the same haploid individual (monoicy) or on two separate haploid individuals (dioicy). Dioicy is the prevalent reproductive system 29 , 32 . This situation contrasts markedly with that described for flowering plants, where only about 6% of extant species have separate sexes, and is more similar to that of bryophytes and liverworts 30 .…”

“…This situation contrasts markedly with that described for flowering plants, where only about 6% of extant species have separate sexes, and is more similar to that of bryophytes and liverworts 30 . Dioicous brown algae may exhibit a broad range of levels of sexual dimorphism, both at the level of the gametophytes and with respect to the difference between male and female gamete size 29 , 32 . While the predicted ancestral state in the brown algae is dioicy, transitions to monoicy have occurred frequently and independently in different clades 32 , 33 .…”

“…Dioicous brown algae may exhibit a broad range of levels of sexual dimorphism, both at the level of the gametophytes and with respect to the difference between male and female gamete size 29 , 32 . While the predicted ancestral state in the brown algae is dioicy, transitions to monoicy have occurred frequently and independently in different clades 32 , 33 . The independent emergence of monoicous lineages from dioicous ancestors makes this group particularly interesting to examine the genomic consequences and mechanisms underlying the breakdown of dioicy.…”

Parthenogenesis and the Evolution of Anisogamy

“…However, if a compatible mate is not encountered, unfertilised gametes of many Ectocarpus species can nevertheless ensure reproductive success by forming a parthenosporophyte that can grow vegetatively, instigating the haploid gametophytic stage of the life cycle [31]. Gamete size is recognised as one of the key factors that may determine whether a gametes are capable of undergoing such parthenogenesis (apomixis), with parthenosporophyte production being restricted to large (female) gametes in many anisogamous species, but also possible in smaller (male) gametes in many species in which anisogamy is mild [32,33]. Interestingly, a recent study in giant kelp (which are closely related to Ectocarpus [34]) identified a genetically male strain that was capable of parthenogenesis [35] via gametes that were on average half the size of those produced by females.…”

“…Taken together, this suggests that at least in principle, the propensity of either sex to reproduce parthenogenically may be more labile than commonly assumed. Categorical descriptions of such possibilities for parthenogenic reproduction in isogamous and anisogamous species across the brown algae can be found in [27,33], while a thorough discussion of empirical results relevant for the following theoretical treatment is provided in [25] for both brown and green algae.…”