Haploid-diploid life cycles are not only good exercise for the brain, but they’re also fantastic study systems to investigate a myriad of questions.
Yet, the majority of molecular studies have focused on the diploid-dominated life cycles of animal and plant taxa. In these organisms, the meiotically-produced haploid gametes immediately fuse to form a new diploid individual. In other words, the haploid stages never become functional, independent organisms.
In contrast, seaweeds, mosses, ferns and some fungi, have life cycles in which there is an alternation between separate, free-living individuals that differ in ploidy levels and reproductive modes. Unlike diploid-dominant plants and animals, the haploid stage in a haploid-diploid life cycle becomes an independent, functional organism with somatic development. Mature haploid adults produce female and/or male gametes that fuse to produce new diploid individuals. The mature diploids undergo meiosis, in which spores are produced and develop into new haploid individuals. Thus, each phase is dependent on the other to complete the sexual life cycle.
What impacts do these life cycles have on genetic structure or on mating systems? Is dioecy really a good proxy for outcrossing in these species (e.g., intergametophytic selfing can still occur, Klekowski 1969)? Why are they maintained, when theoretically, selection should eventually favor either diploidy or haploidy, but not both (Mable & Otto 1998).
There are many variations on the haploid-diploid theme found in mosses, ferns, fungi and seaweeds. As mentioned in this post in the context of colonizing species, we also have a very preliminary understanding of mating system variation and genetic structure in these organisms.
As a mini-review, I’ve compiled a brief summary of what we know, with a slight emphasis on seaweeds (unsurprisingly).
Moss life cycles are dominated by the haploid-stage in which the sporophyte stage remains on the gametophyte.
In mosses, the sperm are free-swimming and fertilization will likely only occur between individuals in close proximity. In addition, due to the leptokurtic distribution of spore dispersal, a female gametophyte will likely be surrounded by sibling haploid progeny from the same sporophyte (Gunnarsson et al., 2007). Consequently, mating is likely to occur among haploid siblings that may be morphologically distinct entities, but is analogous to sefling in diploid organisms (Klekowski 1969).
As briefly reviewed in Krueger-Hadfield et al. (2015), selfing rates (e.g., Taylor et al. 2007), inter-mate distances (van der Velde et al. 2001) and one of the only studies in which correlates of sexual reproduction and life history traits have been investigated in haploid–diploid organisms have been explored in mosses (Crawford et al. 2009).
Szövényi et al. (2009) explored polyandry (multiple paternity) in the dioecious peatmoss Sphagnum lescurii.
Multiple paternity [was] prevalent among sporophytes … Despite significant spatial genetic structure in the population, suggesting frequent inbreeding, the number of inbred and outbred sporophytes was balanced, resulting in an average fixation coefficient and population level selfing rate of zero … Furthermore, female gametophytes preferentially supported sporophytes with higher heterozygosity … Preferential maternal support of the more heterozygous sporophytes suggests active inbreeding avoidance that may have significant implications for mating system evolution in bryophytes.
In contrast to the moss life cycle, fern life cycles are dominated by the diploid sporophyte. The gametophytes are small, heart-shaped individuals that live for a short time.
Previous studies in fern reproductive biology have investigated mating system variation (e.g., Soltis and Soltis 1992). Drawing on Baker’s Law (see this post), colonization events may favor selfing genotypes as opposed to obligate out-crossing genotypes. Using four rare fern species, de Groot et al. (2012) found
that intraspecific variation in mating system may be common, at least among temperate calcicole ferns, and that genotypes with high selfing capacity may be present among polyploid as well as diploid ferns … [Their results support] the idea that selection for selfing genotypes may occur during long-distance colonization, even in normally outcrossing, diploid ferns.
Likewise, Bucharová and Münzbergová (2012) found gene flow in tetraploid ferns, which can undergo selfing, is limited. In diploid ferns, or more likely outcrossers, gene flow was extensive.
Billiard et al. (2012) emphasizes the role fungi can play in investigating mating system variability.
A tremendous diversity of reproductive modes and mating systems can be found in fungi, with many evolutionary transitions among closely related species. In addition, fungi show some peculiarities in their mating systems that have received little attention so far, despite the potential for providing insights into important evolutionary questions.
In their review, Billiard et al. (2012) address two main goals. The first was to clarify sexual reproduction in fungi by placing it in an evolutionary perspective while simultaneously explaining the costs and benefits of the different reproductive modes. The second was to provide the types of analyses that could be implemented in fungi to
help disentangle hypotheses about the evolution of the mode of reproduction and mating systems.
They conclude with a short list of questions that can be addressed using population genetics, phylogenetics and experimental approaches:
Do many species undergo sexual reproduction through haploid selfing? And in this case, why is it so, while they are able of performing asexual reproduction? Are benefits of recombination sufficient to explain the evolution of heterothallism, with the evolution of complex molecular mechanisms restricting syngamy between identical haploids?
Fucoid life cycles are the easiest to remember when taking a phycology class as the sole free-living phase is diploid. Adults produce either or both egg and sperm, depending on whether the species is dioecious or monoecious.
Though, fucoids do not alternate between free-living haploid and diploid stages, there has been a significant contribution to a variety of ecological and evolutionary questions in the genus Fucus. There has likely been a recent and rapid evolution (e.g., Serrão et al. 1999, Coyer et al. 2006) and Fucus species are still capable of hybridization (e.g., Coyer et al. 2002, Billard et al. 2005, Engel et al. 2005). Billard et al. (2010) studied habitat-driven selection within the intertidal zone in the species complex F. vesiculosus L./F. spiralis L. They found 2 genetic entities in F. spiralis with distinct vertical distributions along the intertidal gradient.
Patterns of genetic divergence suggest different times and pathways to reproductive isolation. Divergence between F. vesiculosus and the F. spiralis complex seems to have occurred first, coinciding with divergence in reproductive mode; dioecy versus selfing hermaphroditism. Later, in the hermaphroditic lineage, parallel evolution of 2 co-occurring genetic clusters may have been driven by natural selection and facilitated by high selfing rates in the F. spirals complex (Billard et al. 2010).
Kelps are the foundation species in marine forests and are subject to threats from invasive species and over-harvesting to name a few. They are also emblematic of hetermorphic, haploid-diploid life cycles. The diploid sporophyte is macroscopic (what you think of when you think of a kelp forest) and the haploids sporophytes are microscopic.
Due to this huge difference in size, gametophytes are really hard to sample. Out of necessity, the kelp genetic structure literature is based on the genotyping of sporophyte, and thus, the combined result of zoospore (spores that produce gametophytes) and sperm (egg is retained on female thallus) dispersal.
Nevertheless, current patterns and the availability of substrata have been found to be important drivers of population genetic structure (e.g., Billot et al. 2001, Alberto et al. 2011, Coleman et al. 2011). Oppliger et al. (2014) demonstrated a tendency of geographic parthenogenesis in L. digitata range edge populations. However, this pattern was thought to be due to maladaptation and not an adaptation to life in a marginal habitat. Finally, Voisin et al. (2005) traced the mechanisms of introduction and spread of the invasive kelp Undaria pinnatifida, otherwise known as wakame.
Robuchon et al. (2014) described a method of combined culturing and barcoding of the gametophytic “seed” bank. Gametophytes were cultivated in the laboratory to enable gametogenesis and then the sporophytic recruits were identified to species level. Future work could make use of the availability of more powerful tools with which to incorporate the microscopic gametophyte stage, rather than only looking at the sporophytic stage (e.g., SCG, single cell genomics, see this post).
Red seaweeds have a unique life cycle amongst the haploid-diploid cohort of organisms. Genetically-speaking, the red algal life cycle is biphasic with the alternation of two different ploidies, the diploid sporophytes (called tetrasporophytes) and the haploid gametophytes. Unlike other life cycles, there is a third phase, the carposporophyte (or the cystocarp) that is found on the female thallus in which a zygote is mitotically amplified through a polyembryonic process. The resulting diploid spores from a single cystocarp are genetically identical and settle to form the diploid free-living stage.
Yet, what consequences does this zygotic amplification have on genetic diversity? In theory, every single carpospore can germinate into a tetrasporophyte. Therefore, we might expect to find thousands of tetrasporophytes sharing the same genotype, either stemming from the same cystocarp or a different cystocarp, but same male and female pair.
Moreover, red algal fertilization success was thought to be so poor due to the lack of motile male gametes, the short viability of the male gametes and the retention of the female gamete on the maternal thallus. Thus, the zygotic amplification in the cystocarp maximized a rare, but successful fertilization event.
Engel et al. (1999, 2004) were the first to provide a detailed shorescape view of genetic structure and male gamete dispersal in the red seaweed Gracilaria gracilis. Tidal height had a significant impact on genetic structure in which the high shore populations were more isolated. Contrary to popular opinion, females were fertilized by an average of six different males for every ten cystocarps!
Krueger-Hadfield et al. (2011, 2013, 2015) provided a second detailed shorescpe view in the red alga Chondrus crispus. Unlike G. gracilis in which individuals are discrete morphological entities, C. crispus forms dense monospecific stands in the mid-intertidal. It is incredibly difficult to discern where one individual ends and the next begins. Nevertheless, tidal height once again had a significant effect on genetic structure where the high shore was more isolated. Perhaps unsurprisingly due to the dense aggregation of individuals, there were, on average, nine different fathers for every ten cystocarps! Certainly, this is only an analysis in two species, with very different distributional patterns, but red algal males don’t saturate a female located right nearby.
But, the other curious thing is the stark difference in mating system between G. gracilis and C. crispus which gamete unions were allogamous and endogamous, respectively. Haploid-diploid life cycles should, perhaps, tend toward endogamy because the haploid stage will expose the genome to selection. More species from different red algal orders should be studied to compare the variation in mating system, not only across species, but also across geographic regions.
Perspectives on haploid-diploid life cycles
I won’t deny my bias in finding these life cycles compelling, but there are several practical applications in light of global changes in biodiversity that warrant further investigation of these haploid-diploid organisms.
For example, kelp forests are extremely important near-shore communities, harboring high species diversity. However, kelps are also intensely harvested along coastlines around the world, not to mention also cultivated at industrial scales in marine farms. Where are the centers of genetic diversity? Do they happen to also be areas of intense harvesting practices? Reproduction might be predominately sexual in some kelps (e.g., Oppliger et al. 2014), but is there mating system variation that might impact responses to increasing temperature or to the invasion of non-native species?
Guillemin et al. (2008) demonstrated profound life history modifications in the red alga Gracilaria chilensis due to farming practices. Algal cultivation has resulted in the loss of the free-living stage, but also has selected for certain diploid genotypes. Guillemin et al. (2014) have argued that due to the lower levels of genetic diversity in Chile, these practices might be driving this species to an extinction vortex. These studies beg the question of industrial scale mariculture practices that may lead to similar life history modifications. What are the evolutionary and ecological impacts of the uncoupling of this life cycle? Might similar processes occur in other haploid-diploid organisms?
Alberto F, Raimondi PT, Reed DC et al. (2011) Isolation by oceanographic distance explains genetic structure for Macrocystis pyrifera in the Santa Barbara Channel. Molecular Ecology, 20, 2543–2554.
Billard E, Serrão EA, Pearson GA, Engel CR, Destombe C, Valero M (2005) Analysis of sexual phenotype and prezy- gotic fertility in natural populations of Fucus spiralis, F. vesiculosus (Fucaceae, Phaeophyceae) and their puta- tive hybrids. European Journal of Phycology, 40, 397–407.
Billard E, Serrao E, Pearson G, Destombe C, Valero M (2010) Fucus vesiculosus and spiralis species complex: a nested model of local adaptation at the shore level. Marine Ecology Progress Series, 405, 163–174.
Billiard S, Lopez-Villavicencio M, Hood ME, Giraud T (2012) Sex, outcrossing and mating types: unsolved questions in fungi and beyond. Journal of Evolutionary Biology, 25, 1020-1038.
Billot C, Engel CR, Rousvoal S, Kloareg B, Valero M (2003) Current patterns, habitat discontinuities and population genetic structure: the case of the kelp Laminaria digitata in the English Channel. Marine Ecology Progress Series, 253, 111–121.
Bucharová A, Münzbergová Z (2012) Gene Flow among Populations of Two Rare Co-Occurring Fern Species Differing in Ploidy Level. PLoS ONE 7, e45855.
Coleman MA, Roughan M, Macdonald HS et al. (2011) Variation in the strength of continental boundary currents determines continent-wide connectivity in kelp. Journal of Ecology, 99, 1026–1032.
Collen J et al (2014) Chondrus crispus: a present and historical model organism for red seaweeds. Pp. 53-89 In: Advances in Botanical Research, Volume 71: Sea Plants, ed. N. Bourgougnon, Elsevier.
Coyer JA, Hoarau G, Oudot-Le Secq MP, Stam WT, Olsen JL (2006) A mtDNA-based phylogeny of the brown algal genus Fucus (Heterokontophyta; Phaeophyta). Molecular Phylogenetics and Evolution, 39, 209–222.
Crawford M, Jesson LK, Garnock-Jones PJ (2009). Correlated evolution of sexual system and life-history traits in mosses. Evolution, 63, 1129–1142.
de Groot GA, Verduyn B, Wubs EJ, Erkens R, During H (2012). Inter-and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing. BMC Plant Biology 12, 3.
Engel CR, Wattier RA, Destombe C, Valero M (1999) Performance of non-motile male gametes in the sea: analysis of paternity and fertilization success in a natural population of a red seaweed, Gracilaria gracilis. Proceedings of the Royal Society B: Biological Sciences, 266, 1879–1886.
Engel CR, Destombe C, Valero M (2004) Mating system and gene flow in the red seaweed Gracilaria gracilis: effect of haploid–diploid life history and intertidal rocky shore landscape on fine-scale genetic structure. Heredity, 92, 289–298.
Engel CR, Daguin C, Serrão EA (2005) Genetic entities and mating system in hermaphroditic Fucus spiralis and its close dioecious relative F. vesiculosus (Fucaceae, Phaeo- phyceae). Molecular Ecology, 14, 2033–2046.
Guillemin M-L, Faugeron S, Destombe C et al. (2008) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: how farming practices favor asexual reproduction and heterozygosity. Evolution, 62, 1500–1519.
Guillemin M-L, Valero M, Faugeron S, Nelson W, Destombe C (2014) Tracing the Trans-Pacific Evolutionary History of a Domesticated Seaweed (Gracilaria chilensis) with Archaeological and Genetic Data. PLoS ONE, 9, e114039.
Krueger-Hadfield SA, Collen J, Daguin-Thiébaut C, Valero M (2011) Genetic population structure and mating system in Chondrus crispus (Rhodophyta). Journal of Phycology, 47, 440–450.
Krueger-Hadfield SA, Roze D, Mauger S, Valero M (2013) Intergametophytic selfing and microgeographic genetic structure shape populations of the intertidal red seaweed Chondrus crispus. Molecular Ecology, 22, 3242–3260.
Krueger-Hadfield SA, Roze D, Correa JA, Destombe C, Valero M (2015) O father where art thou? Paternity analyses in a natural population of the haploid–diploid seaweed Chondrus crispus. Heredity, 114, 185–194.
Mable BK, Otto SP (1998) The evolution of life cycles with haploid and diploid phases. BioEssays, 20, 453–462.
Oppliger LV, Dassow von P, Bouchemousse S et al. (2014) Alteration of Sexual Reproduction and Genetic Diversity in the Kelp Species Laminaria digitata at the Southern Limit of Its Range. PLoS ONE, 9, e102518.
Robuchon M, Couceiro L, Peters AF, Destombe C, Valero M (2014) Examining the bank of microscopic stages in kelps using culturing and barcoding.. European Journal of Phycology, 49, 128–133.
Soltis DE, Soltis PS (1992) The Distribution of Selfing Rates in Homosporous Ferns. American Journal of Botany, 79, 97–100.
Szövényi P, Ricca M, Shaw AJ (2009) Multiple paternity and sporophytic inbreeding depression in a dioicous moss species. Heredity, 103, 394–403.
Taylor PJ, Eppley SM, Jesson LK (2007). Sporophytic inbreeding depression in mosses occurs in a species with separate sexes but not in a species with combined sexes. American Journal of Botany, 94, 1853–1859.
van der Velde M, During HJ, Van de Zande L, Bijlsma R (2001). The reproductive biology of Polytrichum formosum: clonal structure and paternity revealed by microsatellites. Molecular Ecology, 10, 2423–2434.
Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversityacross introduced regions in a brown alga: Aquaculture vs. maritime traffic effects. PNAS, 102, 5432–5437.