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From anisogamy to morphologically different males and females: evolution of sexual dimorphisms
It is largely admitted that the initiation of sexual conflict, sexual selection and “attribution” of sex roles evolved from a cascade of evolutionary events initially arising from anisogamy (Parker, 2014; Schärer et al., 2012; but see Ah-King, 2012). In anisogamous organisms the gamete production strategy is not the same in males and females, with the male producing many more gametes than females. This difference leads to a sexual conflict known as the Bateman principle, where males can increase their reproductive fitness by increasing the number of gametes produced and the number of matings, a strategy that females cannot adopt (Bateman, 1948). The best way for females to increase their fitness is to select the best mate to produce fitter offspring. The eagerness of males and the choiceness of females, together with investment in parental care, are the parameters that define the sex roles. The eagerness of males leads to competition between males for access to females, which is one of the components of sexual selection. Another component of sexual selection is the females’ choice of mate.
Sexual selection was first proposed by Darwin in 1871 to explain how sexual dimorphic traits evolved. As explained above sexual selection acts differently in males and females. In the former, male-male competition for access to females creates sexual selection for the evolution of sexual characters related to attractiveness or the ability to increase mating success or reduce the mating success of other males. The evolution of traits improving the attractiveness of males evolved because of female choosiness (O’Donald, 1980). Female choices are made based on traits that indicate the biological fitness of males. Such indicators are cues for “good genes” that can enhance the fitness of offspring, giving the opportunity for females to invest in the production of “good” offspring. Those “good genes” found in males can directly benefit females by improving parental care or by providing females with good territories (e.g.,Williams, 1966; Orians, 1969), but they can also benefit the offspring by providing them with good genes (Grafen, 1990; Hamilton and Zuk, 1982; Zahavi, 1975). This “good gene” benefit is known as the “runaway” process when it involves sexually selected characters because females produce sons that are themselves enhanced in their attractiveness. Such processes lead to the evolution of male ornaments, such as the tail of male peacock.
Using the brown algae to study the evolution of the sexes
Brown algae are photosynthetic organisms found almost exclusively in marine environments, with the majority of species diversity being found in cold water regions. Brown algae are mainly found in the intertidal zones, which is a particularly stressful environment (important abiotic variations), leading to many interesting adaptations. Brown algae are one of the rare groups where complex multicellularity has evolved, and produce an astonishing diversity of morphologies, ranging from microscopic organisms to seaweeds that may attain 50 meters long. These large brown macroalgae, also known as kelps, are of important ecological importance because they create sub-marine forests that shelter an important diversity of organisms. In addition to their ecological interest, brown algae have an important economic interest, with a wide range of uses from food to research for active molecules (McHugh, 2003).
The evolutionary position of brown algae has also stimulated research on this group. Brown algae belong to the Stramenopiles, a group which is phylogenetically almost as distant from the green lineage (Archaeplastidia) as it is from animals (Opishokonts) (more than 1 billion years; Figure 4). This distant phylogenetic position is particularly interesting to assess the universality or novelty of some of the processes driving the evolution of sex determination.
Brown algae display a diversity of types of sexual system
An additional advantage of the brown algae, in the context of the evolution of sex determination, is the fact that they exhibit both an extraordinary diversity of types of life cycle and a wide range of different sexual systems (Luthringer et al., 2014; Silberfeld et al., 2010).
For example, sexuality is expressed during the diploid phase of the life cycle in brown algae with diploid life cycles (dioecy) such as the fucoids, whereas it is the haploid gametophyte generation that exhibits sexuality (dioicy) in algae such as Ectocarpus, that have haploiddiploid life cycles (Luthringer et al., 2014). The selective pressures leading to the evolution of these different systems are distinct: whilst dioecy might evolve from monoecy to limit inbreeding (due, in the latter, to the fertilisation of female gametes by male gametes produced by the same organism), this is unlikely to be the case for dioicy because deleterious mutations should be efficiently purged during the extensive haploid phase of the life cycle. Similarly, genetic sex determination is expected to operate differently, with XY or ZW systems occurring in dioecious species but UV systems occurring in dioicous species. When the different types of brown algal life cycle are mapped onto a phylogenetic tree, the distribution pattern suggests that there has been considerable switching between different life cycle strategies and sex chromosome systems during the evolution of this group (reviewed in Cock et al., 2014). Phylogenetic analysis indicates that dioicy was the ancestral state in the brown algae, and the transition to dioecy presumably required an intermediate state of co-sexuality (e.g. monoecy) with epigenetic sex differentiation (as opposed to genetic sex determination).
Brown algae exhibit a broad diversity of levels of sexual dimorphism
Several sexually dimorphic traits have been described in brown algae (Luthringer et al. 2014). These can be divided into two main classes: 1) differences between male and female gametes and 2) differences between the male and female gamete-producing stage of the life cycle (the gametophyte generation in species with haploid-diploid life cycles). Brown algae exhibit, within a monophyletic group, a broad range of levels of gamete sexual dimorphism, ranging from isogamy (e.g. Scytosiphon lomentaria) to oogamy (e.g. Fucus) (Annexe1: Luthringer et al., 2014). The phylogenetic distribution of gamete size dimorphism has led to the surprising hypothesis that oogamy was the ancestral state in brown algae (Silberfeld et al., 2010). If this hypothesis is correct, it suggests that it may be possible for oogamy to evolve towards isogamy, despite the fact that this type of transition is difficult to explain from a theoretical point of view (see in this Chapter section III.b and Togashi et al., 2012). Interestingly, gamete size differences in anisogamous and oogamous brown algal species are likely to determine whether a gamete is capable of parthenogenesis. Usually both male and female gametes of isogamous brown algal species are capable of parthenogenesis, whereas only the female gametes of anisogamous species are parthenogenetic (i.e. in the latter parthenogenesis is a sexually dimorphic trait; see Clayton and Wiencke, 1990; Ramirez et al., 1986 for exceptions). In oogamous species, the large female gamete is specialised for zygote production and is no longer capable of initiating parthenogenetic development.
Female and male gametophytes can also exhibit sexual dimorphisms. In the orders Laminariales, Desmarestiales, Sporochnales, and Tilopteridales microscopic gametophytes exhibit significant sexual dimorphisms, with females being composed of large cells and males of small cells. This dimorphism allows the morphological identification of females and males in these orders (Müller et al., 1985; Sauvageon, 1915; Schreiber, 1932). Sexes can also exhibit differences in terms of the timing of sexual maturation. In male gametophytes of the kelp Alaria crassifolia antheridia ripen after 4 days under favourable conditions, whereas females require 10 days (Nakahara and Nakamura, 1973). In some cases gametophytes exhibit their sexual dimorphisms under specific, usually extreme, environmental conditions. For instance temperature can differentially influence the survival of male and female individuals of some species (Cosson, 1978; Funano, 1983; Lee and Brinkhuis, 1988; Nelson, 2005; Norton, 1977; Oppliger et al., 2011). Salinity is another abiotic factor that may influence the sex ratio of some brown algae (Norton and South, 1969; Valeria Oppliger et al., 2011).
In brown algae the level of sexual dimorphism is relatively low in comparison with animals, a situation similar to that found in land plants. On the latter it was hypothesized that the low level of sexual dimorphisms is due to the recent evolution of dioecy, and therefore the lack of sufficient time for sexual selection to establish extensive sexual dimorphisms (Barrett and Hough, 2013). However, in brown algae dioicy probably evolved much earlier (Figure 1 in annexe 1), and therefore the latter hypothesis is unlikely to explain the apparent low level of sexual dimorphism in brown algae. Nevertheless, the reproductive biology of brown algae can account for the absence of ostentatious sexual dimorphisms. Indeed, in animals sexes have direct contact with each other allowing sexual selection to strongly affect male and female behaviour and shape sexual dimorphisms (see this Chapter section III.c for more details). On the contrary, in brown algae sexes release their gametes into the surrounding medium (broadcast spawning) and there is only indirect contact between sexes, which provides less opportunity for sexual selection to occur. Consistent with this idea, it was shown that in broadcast spawning organisms, the level of sexual dimorphism is lower than in organisms that have direct contact between sexes during copulation (Levitan, 1998; Strathmann, 1990).
The PAR exhibits structural characteristics that are typically observed in nonrecombining regions of the genome
A number of structural features of the Ectocarpus PAR region, including TE and gene density and gene structure parameters such as exon size, intron size and GC content of the CDS, were intermediate between the values measured for autosomes and for the non-recombining SDR. Moreover, PAR genes were also expressed at lower levels, on average, than autosomal genes and comparisons with orthologues in other Ectocarpus species indicated higher rates of both synonymous and non-synonymous substitutions (and higher dN/dS ratios) in the PAR genes compared with autosomal genes. All of these features are typical of genomic regions that exhibit reduced levels of genetic recombination (5) but, paradoxically, the mean recombination rate measured for the PAR was not significantly different from that of the autosomal part of the genome. Moreover, we found no evidence that PAR genes, on the whole, contained higher levels of sub-optimal codons than autosomal genes (but note that PAR gene coding regions are significantly shorter than those of autosomal genes and this might counteract any tendency for sub-optimal codons to accumulate, because selective pressures on codon usage are typically stronger for genes that encode short proteins (32)). We considered possible evolutionary mechanisms that might explain the unusual structural and functional features of the PAR and its constituent genes. Genetic linkage to the SDR is expected to influence the evolution of the PAR, but the effect should be limited to regions of the PAR that are very close to the SDR (11). This was not the case for the Ectocarpus PAR, as the unusual structural features were characteristic of the entire PAR and were not limited to regions adjacent to the SDR. To date, no mechanisms have been proposed which would allow the SDR to influence the evolution of linked, recombining regions over the distances observed here. It is not clear at present, therefore, whether the unusual structural features of the Ectocarpus PAR are related in some way to the presence of the SDR on the same chromosome or if they indicate that the evolutionary history of the PAR has been different from that of the other autosomes. Similar features, in particular enrichment in TEs, have been observed for the human PAR1, which is of similar size (2.7 Mbp) to the two pseudoautosomal regions in Ectocarpus but associated with a much larger SDR (15, 33), but it has not been reported whether this phenomenon was limited to the part of the PAR that was adjacent to the SDR. To further explore the unusual features of the Ectocarpus PAR, it will be of interest to determine whether this region undergoes recombination in other brown algal species.
Table of contents :
Chapter 1. General Introduction
I.! Origin and maintenance of sex
a.! Introduction and definitions
b.! The origin of sex
c.! The maintenance of sex
d.! Asexual reproduction
e.! Eukaryotic sexual life-cycles
II.!Sex determination in eukaryotes
a.! Epigenetic versus genetic sex determination
b.! Environmental sex determination
c.! Genetic sex determination: polygenic versus monogenic systems
d.! Sex chromosomes and their evolution
e.! Types of sex chromosome system
III.!From sex determination to sexual differentiation: the evolution of sexual dimorphisms
a.! Evolution of mating types
b.! Evolution of anisogamy
c.! From anisogamy to morphologically different males and females: evolution of sexual dimorphisms
IV.!Using the brown algae to study the evolution of the sexes
a.! Brown algae display a diversity of types of sexual system
b.! Brown algae exhibit a broad diversity of levels of sexual dimorphism
Objectives
Chapter 2. The Haploid System of Sex Determination in the Brown Alga Ectocarpus sp.
I.! !Introduction
II.!!Paper
III.!Discussion and Perspectives
Chapter 3. The Pseudoautosomal Region on the Ectocarpus UV Sex Chromosomes
I.! Introduction
II.!Paper
III.Discussion and perspectives
Chapter 4. Evolution of Sex-Biased Gene Expression in a Haploid Sex-Determination System with Limited Sexual Dimorphism
I.! Introduction
II.!Paper
III.!Discussion and perspectives
Chapter 5. Genetic Basis of Parthenogenesis, a Sexual Dimorphic Trait in Ectocarpus siliculosus
I.! Introduction
II.!Material and Methods
Brown algal culture
Measurement of parthenogenetic capacity
Preparation segregating populations
DNA extraction and phenotyping the segregating population
Sequencing genomic data
SHOREmap analysis
Genotyping candidate regions
Fitness measurement
Measurement of gamete size
III.!Results
Phenotypic characterization
Analysis of a segregating population
Parthenogenesis is a genetically controlled trait
SHOREmap analysis indicated candidate regions preferentially on the PAR
Analysis of the fitness of P+ and P- male gametes
Gamete size and parthenogenetic capacity
Parthenogenetic capacity of diverse Ectocarpus strains and species
IV.!Discussion and perspectives
Chapter 6. Insights into the cellular basis of parthenogenesis in Ectocarpus
I.! Introduction
II.!Material and Methods
Algae material and culture
Treatments with inhibitors
Microscopy
III.!Results
Transcription inhibitors do not affect germination nor the first cell division but do
prevent further development of Ectocarpus partheno-sporophytes
Emetine prevents the first cell division in Ectocarpus partheno-sporophytes .
Early treatment with translation inhibitor results in abnormal patterning of
Ectocarpus partheno-sporophytes
IV.!Discussion and perspectives
Chapter 7. General Conclusions and Perspectives
Bibliographie
