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Evolution from Mating types to different sexes


Imagine a lineage of multicellular organisms that had mating types and evolved their mating types into sexes. What are the possible mechanisms that might have brought this lineage to evolve sexes from mating types?

To my understanding of the definitions of sexes and mating types, the only diffenece between the two is that sexes imply gametes of different sizes. Is it correct?


Another important reason to have mating types is to prevent self-fertilization or self-polination that produces less capable offspring. Because of this requirement, mating types may evolve also for species that produce both types of gametes, or does not differentiate them into male and female gametes. Fertilization is only possible if gametes have different mating types.

It may be more than two mating types, but if there are only two, they are probably similar to "sexes" even if gametes do not look different.


Sexual Dimorphism and Selection Selection

When we consider the question “why sex?”, one answer stems from the evolutionary benefits to intermingling genes with the genes of a chosen mate to maximize the awesomeness of the children and their future children. In evolutionary terms, the children’s awesomeness is entirely based on their survival and ability to reproduce viable, fertile offspring—in other words to provide grandchildren. Biologists have studied the evolutionary strategies that maximize survival and reproduction.


Introduction

In many organisms, sexual reproduction occurs only between distinct mating types. Dimorphic sex chromosomes define two mating types in most mammals, with dozens to hundreds of alleles determining hundreds to thousands of mating types in some plants and fungi. Recent information on the genomic structure of mating type regions, notably the human Y chromosome, has contributed to an emerging paradigm of mating type evolution. Here I address the origin and evolution of mating type regions, with particular consideration of the determinant of mating type in angiosperm self-incompatibility (SI) systems (S-locus). The various processes involved in the evolution of mating type proceed in parallel among the multiple mating types segregating in SI systems.


On Forces of Selection in the Evolution of Mating Types

The origin, multiplication, and limitation of numbers of mating types in theoretical, primitive eucaryotic protists are considered in the context of interindividual selection. Mating types may have evolved in response to selection for outbreeding when random mating often resulted in inbreeding and individuals of different mating types were on average more genetically different than individuals of the same type. Sexual selection probably originated with mate choice in primitive eucaryotic protists. More than two mating types may persist in some populations because acceptability as a pairing partner to as many other individuals as possible may be advantageous, and/or the advantages of outbreeding may be partly countered by the advantages of adaptation to particular environments the latter advantage is most likely to exist in a population subdivided into relatively severe but predictable habitat patches. The maximum number of mating types in a population is probably limited by selection against genetically incompatible pairings, competition between members of different mating types, and the between-sexes-choice form of sexual selection operating against genetically incompatible and/or competitively inferior individuals.


Pseudohomothallism and Evolution of the Mating-Type Chromosome in Neurospora Tetrasperma

Ascospores of Neurospora tetrasperma normally contain nuclei of both mating-type idiomorphs (a and A), resulting in self-fertile heterokaryons (a type of sexual reproduction termed pseudohomothallism). Occasional homokaryotic self-sterile strains (either a or A) behave as heterothallics and, in principle, provide N. tetrasperma with a means for facultative outcrossing. This study was conceived as an investigation of the population biology of N. tetrasperma to assess levels of intrastrain heterokaryosis (heterozygosity). The unexpected result was that the mating-type chromosome and autosomes exhibited very different patterns of evolution, apparently because of suppressed recombination between mating-type chromosomes. Analysis of sequences on the mating-type chromosomes of wild-collected self-fertile strains revealed high levels of genetic variability between sibling A and a nuclei. In contrast, sequences on autosomes of sibling A and a nuclei exhibited nearly complete homogeneity. Conservation of distinct haplotype combinations on A and a mating-type chromosomes in strains from diverse locations further suggested an absence of recombination over substantial periods of evolutionary time. The suppression of recombination on the N. tetrasperma mating-type chromosome, expected to ensure a high frequency of self fertility, presents an interesting parallel with, and possible model for studying aspects of, the evolution of mammalian sex chromosomes.


The adaptive significance of sex

When two reproductive cells from somewhat unlike parents come together and fuse, the resulting product of development is never exactly the same as either parent. On the other hand, when new individuals, plant or animal, develop from cuttings, buds, or body fragments, they are exactly like their respective parents, as much alike as identical twins. Any major change in environmental circumstances might exterminate a race since all could be equally affected. When eggs and sperm unite, they initiate development and also establish genetic diversity among the population. This diversity is truly the spice of life and one of the secrets of its success sex is necessary to its accomplishment.

In each union of egg and sperm, a complete set of chromosomes is contributed by each cell to the nucleus of the fertilized egg. Consequently, every cell in the body inherits the double set of chromosomes and genes derived from the two parental cells. Every time a cell divides, each daughter cell receives exact copies of the original two sets of chromosomes. The process is known as mitosis. Accordingly, any fragment of tissue has the same genetic constitution as the body as a whole and therefore inevitably gives rise to an identical individual if it becomes separated and is able to grow and develop. Only in the case of the tissue that produces the sex cells do cells divide differently, and genetic differences occur as a result.

During the ripening of the sex cells, both male and female, cell divisions (known as meiosis) occur that result in each sperm and egg cell having only a single set of chromosomes. In each case the set of chromosomes is complete—i.e., one chromosome of each kind—but each such set is, in effect, drawn haphazardly from the two sets present in the original cells. In other words, the single set of chromosomes present in the nucleus of any particular sperm or egg, while complete in number and kinds, is a mixture, some chromosomes having come from the set originally contributed by the male parent and some from the female. Each reproductive cell, of either sex, therefore contains a set of chromosomes different in genetic detail from that of every other reproductive cell. When these in turn combine to form fertilized eggs or fertile seeds, the double set of chromosomes characteristic of tissue cells is reestablished, but the genetic constitution of all such cells in the new individual will be the same as that of the fertilized egg—two complete sets of genes, randomly derived from sets contributed by the two different parents. Variation is thus established in two steps. The first is during the ripening of the sex cells, when each sperm or egg receives a single set of chromosomes of mixed ancestry. None of these cells will have exactly the same combination of genes characteristic of the respective parent. The second step occurs at fertilization, when the pair of already genetically unique sex cells fuse together and their nuclei combine, thus compounding the primary variation.


General Overviews

The relative advantages of inbred and outbred mating systems in plants have been discussed since at least the 19th century. Barrett 2010 provides a detailed account of Darwin’s thoughts on mating system. In the 20th century, a series of canonical models for the evolution of self-fertilization arose from the field of population genetics. Charlesworth and Charlesworth 1979 clearly outlines the sequence of important models until the late 1970s, and Jarne and Charlesworth 1993 includes all current major models. Parallel to the development of theory, descriptive science has expanded the corpus of knowledge on the distribution of mating systems among taxa. Fryxell 1957 reviews mating system diversity in depth. Because both selfing and asexual reproduction require only a single parent, it is easy to conflate the two. Holsinger 2000 explains the key differences between selfing and asexual reproduction.

Barrett, Spencer C. H. 2010. Darwin’s legacy: The forms, function and sexual diversity of flowers. Philosophical Transactions of the Royal Society of London B: Biological Sciences 365:351–368.

This high-level review evaluates adaptive explanations of the morphological diversity of flowers. It extensively catalogs different types of floral adaptations, including those that are less well known. The author traces modern discussion of the topic back to Darwin, who explained most floral adaptations as a means of maximizing outcrossing.

Charlesworth, Deborah, and Brian Charlesworth. 1979. The evolutionary genetics of sexual systems in flowering plants. Proceedings of the Royal Society of London B: Biological Sciences 205:513–530.

The authors review the development of concepts in a chronological sequence of canonical models and relate how each built on previous work. This article provides the clearest view available of the historical context of models published previously.

Fryxell, Paul A. 1957. Mode of reproduction of higher plants. The Botanical Review 23:135–233.

This taxonomically broad review classifies angiosperm mating systems based on frequency of cross-fertilization, self-fertilization, and asexual reproduction through seed (see Outcrossing Rate). It gives a sense of the proportions of species practicing these forms of reproduction.

Holsinger, Kent E. 2000. Reproductive systems and evolution in vascular plants. Proceedings of the National Academy of Sciences 97:7037–7042.

This review provides an introduction to the population genetic consequences of mating system in land plants. In particular, the comparison of the effects of self-fertilization and asexual reproduction reveals important symmetries while pointing out potential sources of confusion between them.

Jarne, Philippe, and Deborah Charlesworth. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annual Review of Ecology and Systematics 24:441–466.

The authors of this review recommend a reorientation of mating system research toward an empirical focus. They argue that the possible theoretical advantages of selfing and outcrossing have been exhaustively described, but that basic data on selfing rate, inbreeding depression, and inbreeding coefficients are insufficient to decide their importance. The authors also explain the uses and limitations of some of the methods of estimating these parameters.

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Gamete signalling underlies the evolution of mating types and their number

The gametes of unicellular eukaryotes are morphologically identical, but are nonetheless divided into distinct mating types. The number of mating types varies enormously and can reach several thousand, yet most species have only two. Why do morphologically identical gametes need to be differentiated into self-incompatible mating types, and why is two the most common number of mating types? In this work, we explore a neglected hypothesis that there is a need for asymmetric signalling interactions between mating partners. Our review shows that isogamous gametes always interact asymmetrically throughout sex and argue that this asymmetry is favoured because it enhances the efficiency of the mating process. We further develop a simple mathematical model that allows us to study the evolution of the number of mating types based on the strength of signalling interactions between gametes. Novel mating types have an advantage as they are compatible with all others and rarely meet their own type. But if existing mating types coevolve to have strong mutual interactions, this restricts the spread of novel types. Similarly, coevolution is likely to drive out less attractive mating types. These countervailing forces specify the number of mating types that are evolutionarily stable.

This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.

1. Introduction: why have distinct mating types and how many?

While sexual reproduction requires two parents, there is no obvious need for them to be differentiated into distinct mating types or sexes. Yet, this is the predominate state of nature, from complex birds, mammals and plants down to humble single-celled eukaryotes. Sexual reproduction in complex organisms is contingent upon highly specialized male and female roles both at the organismal level (e.g. sex-specific attraction mechanisms) and cellular level (e.g. egg and sperm motility and size differences).

This picture changes when considering unicellular organisms. Although an asymmetry in gamete size (anisogamy) exists in some unicellular taxa, the vast majority of unicellular protist gametes are morphologically identical (isogamy) [1]. Yet the gametes of isogamous species are divided into genetically distinct mating types. These mate disassortatively, scarcely ever with members of the same type. This arrangement is paradoxical as it comes with a major cost since it restricts the pool of potential partners to those of a different mating type. Furthermore, this cost is maximized with two mating types, which perplexingly is the most common state in nature among isogamous organisms.

Considerable effort has been expended in forming and testing hypotheses to explain the evolution of mating types [2]. A prevalent explanation drawn from the literature on multicellular organisms suggest that mating types serve to avoid inbreeding by preventing matings between members of the same clone [3–6]. Another notable hypothesis proposes that mating types evolved because different gamete types can enforce uniparental inheritance of the cytoplasm, thereby restricting the spread of mitochondrial mutations or selfish elements [7–11]. Both are persuasive ideas but not without problems. The key challenge to both of them is the presence of several species where inbreeding and biparental inheritance is the rule but that nonetheless maintain mating types [12]. For example, in budding yeast the parent is diploid (heterozygous for the mating types alleles a and α) and undergoes meiosis to produce four haploid spores, two of each mating type. The spores then germinate and mate within the same tetrad while inheriting cytoplasm from both parents. Similar behaviour is encountered in a variety of other groups (e.g. Neurospora tetrasperma, Gelasinospora tetrasperma, Podospora anserina and P. tetraspora [13]).

We do not consider these theories further here, as they have been subject to several recent reviews [2,12,14]. Instead we focus and expand a neglected hypothesis first proposed by Hoekstra [15]. He suggested that mating types are determined by the molecular system regulating gamete interactions. The underlying idea is that partner recognition and pairing are more efficient when gametes produce recognition/attraction molecules and their receptors in a mating-type-specific manner. Indeed, in the absence of any asymmetry, cells will saturate their own receptors and compromise their ability to detect and find partners [12,16]. This is a compelling idea bringing cell–cell signalling to the centre of mating-type evolution.

The evolution of sexual signalling and mating preference has received great attention among multicellular organisms [17]. However, the same processes in the unicellular world have been barely addressed, particularly among isogamous species lacking obvious differentiation. This neglect in part reflects the popular assumption that opposite mating-type fusions exist for reasons unrelated to the signalling interaction itself (e.g. inbreeding avoidance and control of organelle inheritance, as discussed above). In addition, it is generally assumed that sex-specific roles follow from asymmetry in gamete morphology and motility (e.g. [18]), and this has overshadowed consideration of asymmetric signalling among isogamous species. To rectify this imbalance, we review signalling between gametes in isogamous species and show that asymmetry in gamete communication is universal. We argue that this asymmetry's primary function lies in promoting mating success. We then develop a simple model of gamete signalling and mating-type evolution that explains why the number of mating types is so frequently restricted to two and provides conditions under which more numerous mating types are favoured.

2. Review: gamete signalling

In unicellular organisms, sex is initiated when individuals (vegetative cells) are subject to growth arrest and produce sex-competent cells, either through meiosis (in diplontic species) or differentiation into gametes (in haplontic species figure 1). This occurs as a response to environmental cues and/or substances released by other individuals of the same species. Following sexual differentiation, gametes must find and recognize other sex-competent cells of the same species, form adhesion and conjugation pairs, and synchronously permit fusion (figure 1). Here, we review gamete signalling interactions in unicellular and some multicellular species with isogamy, and point out the role of mating-type asymmetry.

Figure 1. Model life cycle for unicellular eukaryotes. Cells grow vegetatively for as long as conditions allow. Entry into the sexual phase begins with growth arrest (1) followed by differentiation into gametes (2). Diplontic species undergo meiosis to produce haplontic gametes, whereas haploid species simply differentiate into sex-competent cells. Gametes or sex cells encounter one another (3), either by chance (e.g. Chlamydomonas reinhardtii), via directed growth following diffusible pheromones (e.g. yeasts) or through sexual chemotaxis (e.g. Closterium). When cells come in contact they recognize and adhere to one another (4). This is followed by cell and nuclear fusion (5). The diploid zygote then switches back to the vegetative programme in diplontic species or undergoes meiosis to produce haploid vegetative cells.

(a) Algae

(i) Chlamydomonas

Chlamydomonas species are biflagellate algae with two mating types (MT + and MT − ) and are generally isogamous. Haploid vegetative cells differentiate into gametes when environmental nitrogen levels drop [19]. The MT locus is located in a chromosomal region carrying several large inversions and translocations that suppress recombination. The MT + and MT − variants contain a number of genes that code for differentiation into + or – gametes, including mating-type-specific agglutinins that act as recognition and adhesion molecules. When gametes of the opposite mating type meet the agglutinins along their flagella interlink and adhere. Adhesion initiates a cascade that results in a 10-fold increase in intracellular cAMP, which enhances agglutinin levels and flagellar adhesiveness [20–22]. It also leads to the release of lytic enzymes that lead to rapid gamete cell wall disassembly and simultaneous production of complementary mating structures that prepare the gametes for fusion (figure 2a) [23–25]. Individual cells develop mating structures and fusion competence when exposed to conspecific substances even in the absence of a partner, pointing at the pivotal role of agglutinins in the mating process [25]. Following fusion, the two gametes contribute distinct information that is necessary for zygote development by forming heterodimers between the transcription factors Gsm1 and Gsp1 that are expressed differentially in the two mating types [19]. The heterodimers initiate zygote differentiation and meiosis. There is also evidence for sexual chemotaxis in some species of Chlamydomonas. At least one of the two mating types is attracted to substances released by the other type, but the putative substances have not been isolated or characterized [26,27].

Figure 2. (a) Two Chlamydomonas cells undergoing fusion. Picture reproduced from Goodenough & Weiss [24] with permission from the authors. (b) Tetrahymena cells conjugating in preparation for nuclear exchange. Picture credit: SEPA ASSET programme at Cornell University.

(ii) Closterium

Closterium are diploid green algae and the closest unicellular relatives to land plants. Most Closterium species have two mating types, mt + and mt − . Their sexual reproduction is well characterized and takes place in five steps: sexual cell division producing sexually competent cells (SCD), cell pairing, conjugation and papillae formation, protoplast release (i.e. loss of the cell wall) and protoplast fusion to produce a zygospore [28]. The presence of chemical substances responsible for coordinating sexual activity was postulated for Closterium species as early as 1971 [29]. It is now known that in the Closterium peracerosum-strigosum-littorale (C. psl) species complex, PR-IP (protoplast release-inducing protein) inducer is secreted by mt − cells which stimulates SCD, protoplast release and mucilage secretion activity in mt + cells [30,31]. The induction activity differs according to the PR-IP inducer concentration: low to mucilage secretion, medium to SCD and high to protoplast release in mt + cells [28]. The same is true for the corresponding mt + substance simulating the equivalent concentration-dependent reactions in mt − cells. Similar multifunction mating type factors have been identified also in Closterium ehrenbergii [32,33]. In addition, mt + and mt − cells of C. ehrenbergii and Closterium acerosum migrate towards one another when separated [34–36]. This suggests the presence of mating-type-specific chemoattraction between opposite types, but these putative substances have not yet been characterized.

(iii) Diatoms

Diatoms have a unique diplontic vegetative phase involving size reduction associated with mitotic divisions [37]. The switch to sexual reproduction only occurs in cells below a critical size. Haploid gametes are generated via meiosis and are unable to grow clonally, so they must fuse to return to the diploid stage (or die). It has long been speculated that diatoms use pheromone signals to coordinate sexual reproduction [37]. Recent work has identified some of the components of this system in the pennate diatom Seminavis robusta. MT + cells produce SIP + , a pheromone that induces cell cycle arrest and gamete production in MT − cells. It also induces proline biosynthesis and release of the pheromone diproline from MT − cells. Diproline acts as a chemoattractant for MT + cells [38,39]. The role of these reciprocal pheromones and other substances in subsequent stages of diatom mating (i.e. recognition and fusion) is not currently known.

(iv) Brown algae

Brown algae are multicellular marine algae. Sexual reproduction can be isogamous, anisogamous (different size gametes) or oogamous (large egg and small sperm). Pheromones in brown algae have been studied extensively and are well characterized in terms of their function and molecular composition [40]. In isogamous brown algae such as Scytosiphon lomentaria, Colpomenia bullosa and Ectocarpus siliculosus, the female-equivalent mating type releases pheromones that attract the male-equivalent mating type [41,42]. In E. siliculosus, mating-type-specific glycoproteins and receptors are responsible for gamete recognition and adhesion [42,43]. While the two mating types of E. siliculosus are morphologically the same, their mating behaviour is different. The + gametes swim for a short period of time after which they ingest their flagella and secrete pheromones. The − gametes, on the other hand, swim for prolonged periods and have pheromone receptor sites for signal processing necessary for their chemotactic response. They recognize the + gametes through receptors on their anterior flagellum, but the details of how this is achieved remain unexplored [43]. Transcriptome profiling of + and – gametes of E. siliculosus demonstrates extensive asymmetry between the two mating types highlighting that distinct sexual roles precede morphological differentiation of gametes [44].

(b) Fungi

(i) Yeasts

Yeasts are isogamous, single-celled fungi, with two mating types. The vegetative stages of yeasts can be predominantly haploid (e.g. Schizosaccharomyces pombe) or diploid (e.g. Saccharomyces cerevisiae). Mating type is determined at the haploid level at a single genetic locus, MAT. The pertinent genes for each mating type are differentially expressed at this locus. The sexual cycles of yeasts begin with growth arrest and differentiation into gametes. This occurs as a response to environmental cues but, in addition, mating-type-specific pheromones initiate gametogenesis when sensed by the opposite type [45]. In both S. pombe and S. cerevisiae, binding to pheromone from the opposite mating type causes expression of mating-type-specific genes, and induces physiological and morphological changes leading to sexual differentiation [45]. Polarization of individual gametes along the pheromone gradient leads to directed growth towards gametes of the opposite mating type [45]. Mating-type-specific pheromones have similar functions in several other yeasts [46–49].

The molecular processes leading to gamete fusion are known in considerable detail [45]. It begins with the induction of mating-type-specific agglutinins by the opposite mating-type pheromone. The interlinking of agglutinins leads to cell adhesion [50,51] and increases conjugation efficiency [52]. Budding yeast mutants unable to produce mating pheromones cannot induce agglutination or conjugation and are effectively sterile [53]. Although exogenous pheromone restores agglutination, it does not lead to conjugation and fusion, suggesting that modulation of the pheromone concentration and the timing of secretion control downstream pathways crucial for mating [53]. As in Chlamydomonas, upon zygote formation transcription factors expressed differentially in the two mating types in yeasts form heterodimers that repress genes involved in mating and the haploid life cycle and are crucial for subsequent zygote development and meiosis [54,55].

(ii) Filamentous ascomycetes

Mating-type genes have also been studied in several filamentous ascomycetes. During sexual development, opposite mating types form male and female structures (defined as the donor and receiving structures, respectively) that fuse with one another allowing the transfer of the male nucleus to the female structure [56,57]. The entry of the male nucleus into the female hyphal cell stimulates fruiting body formation. The nuclei from the two mating types do not fuse but undergo repeated mitotic divisions in synchrony resulting in a fruiting body composed of cells with multiple nuclei from both mating types. The nuclei are then organized into dikaryotic cells, with one nucleus of each mating type, which fuse, and undergo meiosis and spore production.

The mating types regulate directed growth of the female structures towards the male, partner recognition, fertilization, fruiting body formation and nuclear coordination in the fruiting body [56,58,59]. The female trichogynes are attracted towards the male spermatia, suggestive of diffusible pheromones [60–62]. Pheromone precursor genes have been identified in many filamentous ascomycetes including Cryphonectria parasitica [63], Magnaporthe grisea [64], Podospora anserina [65] and Neurospora crassa [66]. The pheromone precursor genes are expressed in a mating-type-specific manner, similar to yeast pheromones. In some species such as Ascobolus, differentiated sexual structures only develop following opposite-mating-types interaction [67]. For example, the male element in A. stercorarius undergoes sexual activation after contact with the mycelium of the opposite mating type [68]. Other filamentous species like P. arsenia have the ability to differentiate sexual structures without mating-type interactions [62]. Interestingly, P. arsenia is a pseudohomothallic species, meaning that a single individual carries both mating types and so compatible partners are always present. This eliminates the need to have a check-point prior to sexual differentiation to ensure the presence of a partner.

A further key role of the mating types is the specification of nuclear identity, coordination of nuclear pairing and migration of nuclei into the dikaryotic hyphal cell [56]. In P. anserina, nuclear recognition is regulated by FMR1 and SMR2 proteins in the mat − nucleus and the FPR1 protein limited to the mat + nucleus. When nuclei of the opposite mating type approach one another they release signals that simulate growth and nuclear migration, the success of this process relying on the proper association between the two nuclei [57,69]. Mutations in these genes affect nuclear synchronization, causing errors in dikaryote formation and barren fruiting bodies [70].

(iii) Filamentous basidiomycetes

Basidiomycetes spend most of their life cycle as dikaryons. Each cell holds two nuclei from the mating partners without fusion, and this state persists during the asexual phase [71]. Mating-type identity is determined by alleles at either one locus (bipolar system) or two unlinked loci (tetrapolar system). In the tetrapolar system, fusion normally only occurs between individuals that differ at both mating-type loci (e.g. A1B1 × A2B2). Basidiomycetes are notable for having multiple mating types ranging from two up to several thousands, with multiple alleles possible at both loci. Mating types mediate pheromone signalling, cell fusion, filamentous growth in the dikaryote phase and preservation of compatible nuclei in close association through synchronized nuclear division [58,59,71].

Heterobasidiomycetes use pheromone signals to mediate mating partner choice, with pheromone interaction with receptors initiating the mating process when haploid isogamous cells or organs of the opposite mating type come in contact. Ustilago hordei has a bipolar mating system and two mating types. Mating-type pheromones in this species induce conjugation and tube formation in opposite mating types that grow chemotactically towards one another [72]. In the related U. maydis, following pheromone binding, mating structures are formed that enable fusion and the formation of the dikaryon. After fusion, mating-type alleles of the two partners form heterodimers that enter the diploid nucleus and control switching to filamentous growth and the subsequent meiosis [73,74]. Remarkably, these tight interactions occur despite U. maydis having some 50 mating types, which are determined at two multi-allelic loci [71].

In homobasidiomycetes (mushrooms), fusion between mycelia occurs independently of mating type. In these fungi, mating-type pheromones are activated following fusion and control formation of nuclear pairs in the dikaryon and maintain the dikaryophase [75]. A notable example is that of Schizophyllum commune that has thousands of mating types. Molecular analyses have found more than 75 different pheromones and several receptors [76]. Each distinct mating type consists of several genes specifying a single pheromone receptor pair [76]. But the receptors within a mating type never bind their own pheromones [77]. The pheromones and receptors control nuclear recognition and fusion within the mycelium [77,78]. A high degree of specificity is required for nuclear communication and the full completion of sexual development [76]. Although the mating system of S. commune restricts sibling matings to some extent, these are still possible approximately 25% of the time, suggesting that inbreeding avoidance cannot be the main function of these complex mating interactions. The situation is similar in other mushroom species such as Coprinus cinereus [79].

(c) Amoebozoan slime moulds

In the cellular slime moulds, the unicellular phase of the life cycle is initiated following spore release from the fruiting body. The spores germinate and release haploid amoeboid cells that grow vegetatively while food supplies are abundant. Under stressful conditions, the unicellular amoebae either aggregate to form a new fruiting body or fuse to form a diploid zygote giant cell known as a macrocyst [80,81]. Macrocysts form through the fusion of cells with different mating types. In the well-studied Dictyostelium discoideum, there are three mating types, one of which appears to be a fusion of the other two [80]. At least two interacting mating-type-specific pheromones are necessary for macrocyst development and completion of the sexual phase [82]. Disruption of the mating-type genes suppresses cell fusion in D. discoideum [83,84]. However, the role of mating-type genes is poorly understood in this and other slime moulds such as D. purpureum and D. giganteum [85,86].

(d) Ciliates

Mating in several ciliate groups does not involve cell fusion. Instead, compatible mating types form conjugating pairs, followed by exchange of nuclei through a conjugation bridge [87]. The conjugants then separate and the nuclei in each cell fuse before restoring the vegetative phase. Ciliates contain two nuclei, the micronucleus and the macronucleus. The diploid micronucleus undergoes meiosis. The ‘somatic’ macronucleus forms from massive rearrangement, amplification and gene loss from the diploid micronucleus.

The number of mating types in the genus Euplotes varies from five to 12 [87]. Many species, including E. octocarinatus, E. raikovi, E. patella and E. woodru, secrete mating-type-specific substances [87,88]. Individual cells grow vegetatively when binding to their own pheromone secreted continuously in the extracellular environment. Mature cells arrest growth and develop mating competence only when they bind to a non-self pheromone. The same substances also act as chemoattractants and sexualized cells are attracted to all non-self pheromones [89–91]. The interaction between mating-type pheromones in several ciliate species also regulates adhesion and conjugation between complementary gametes [91–93]. Some species of Euplotes reportedly do not secrete mating-type substances [87]. Instead, mating-type-specific interactions occur upon contact and prepare cells for conjugation [94]. It is worth noting that more recent reports suggest that E. crassus, a species previously thought to only carry surface-bound pheromones, actually does secrete pheromones but it remains to be seen whether diffusible pheromones are universal in Euplotes [95].

Cell adhesion is mediated through cilia binding via mating-type non-specific adhesins. However, mating-type-specific pheromones and receptors are used to coordinate adhesion and fusion. For example, the ciliate Dileptus margaritifer forms mating pairs due to the expression of mating-type non-specific cell-surface molecules [93]. The two partners coordinate the expression of their adhesion proteins by secreting and responding to pheromones in a mating-type-specific manner. Experiments found that conjugation is highly unstable between gametes of the same mating type [93]. It appears that continued stimulation using pheromones is needed until fusion is completed. Similar results were reported for E. octocarinatus where pairs of the same mating type were able to form under laboratory conditions but were unstable and generally separated before entering meiosis [96].

Paramecium is an exception among ciliates in that sexual cells produce mating-type-specific agglutinins [87]. In the isogamous Paramecium bursaria, mating-type-specific substances are responsible for pair formation, conjugation, adhesion and fusion [97]. The mating reaction following mixing of opposite mating types was observed in a number of different species [98], suggesting that similar substances coordinate mating in a number of different species of Paramecium. However, few details of the molecular signalling interactions are currently known. Finally, sexual chemotaxis does not occur among Paramecia. However, cell movement inactivation was reported following opposite-mating-type contact-mediated interactions [99].

3. The role of signalling asymmetry

Mating is contingent upon a cascade of events orchestrated between the mating cells. Our review of isogamous species reveals that these interactions are universally regulated by mating types, which produce a range of mating-type-specific proteins. These control a number of processes from initial sexual differentiation, through to gamete fusion and subsequent events in somatic development. The interactions between mating types are always asymmetric—a particular mating type will stimulate others (whether there are two or multiple) but always fails to stimulate cells carrying the same mating type. This asymmetry in intercellular signalling during sex appears to be fundamental to the evolution of mating types [12,16]. On what basis is asymmetry important? We address this question for each of the steps in the sexual cycle.

Diffusible signals are at least in part necessary for growth arrest and sexual differentiation in a range of species, including yeasts, ciliates and diatoms. Why cannot all cells send and differentiate in response to the same signal at this stage? Cells would then face the challenge of distinguishing their own signal from that of potential partners [12]. Owing to diffusion, signals from self will always be higher than those of a remote partner, considerably degrading the ability to distinguish self and other signals (figure 3a). Recent experiments have reinforced this idea by showing that secreting and detecting the same molecule can prevent cells from responding to signals from others, particularly at low cell densities [100]. In many species, differentiation into gametes is not reversible and the only way for individuals to restore their mitotic growth phase is by sexual fusion. It is therefore vital that passage into gametogenesis is synchronized with others, who are potential partners.

Figure 3. (a) The concentration profiles around two secreting cells centred at X1 and X2. The local concentration due to own pheromone C11 (blue) or C22 (red) is always higher than that of a remote cell C12 (red) or C21 (blue) at X1 or X2 respectively. A very high density of neighbouring cells would be required to generate concentration profiles that exceed those generated by an individual cell's own secretion. (b) Moving and pheromone sending generate a tail of high concentration behind moving secretors. This would prompt chemotactic cells that move towards one another to reverse their motion, unless they use distinct pheromones.

Following sexual differentiation individuals must pair. The majority of species reviewed here (with the exception of some species of ciliates and some chlamydomonads) use pheromones to direct migration or growth towards one another. Sending and receiving the same chemotactic signal could be problematic due to the potential of receptor saturation [15]. Experimental overexpression of pheromone disturbs gamete polarization in yeast gametes resulting in growth in a random direction, and a 15-fold increase in mating time [101]. An additional problem is that secretion during movement results in high chemoattractant concentration behind moving cells due to diffusion and accumulation of chemical molecules [16]. This alters the net local concentration, reducing the cell's ability to respond appropriately to external signals, or worse prompting the cell to reverse its direction of movement (figure 3b). Consequently, the use of chemotaxis to bring partners together likely provides a substantial advantage if attraction signals are sent and received asymmetrically [16].

Upon physical contact gametes must recognize one another as conspecifics, adhere and proceed to conjugation and/or fusion. There is strong selection for swift initial recognition when there is competition between gametes for example, only two from an initial clump of several cells will mate in Paramecium and Chlamydomonas [19,102]. Furthermore, conjugation and fusion involve cell wall remodelling and must be tightly coordinated, as lack of synchronization can lead to osmotic shock and cell lysis [45]. Several species use the same mating-type pheromone/receptor pairs to induce gametogenesis as well as sexual chemotaxis. This is achieved by shifts in pheromone concentration inducing corresponding shifts in the other mating type's pheromone production. This would be difficult to achieve without asymmetric signals, as distinguishing changes in own versus partner pheromone production would be nigh on impossible (figure 3a). Several species use non-diffusible, surface-bound molecules for adhesion, conjugation and fusion, which are distinct from their pheromones and receptors. These again show mating-type specificity in species like Paramecium and some Chlamydomonas. A probable reason for this asymmetry lies in the avoidance of binding between self molecules that could lead, not only to saturation, but also to noise/interference that could potentially impair fusion synchronization or rapid cell–cell recognition. There is little specific theoretical work on this possibility beyond Hoekstra's original work [15], though cell surface interactions likely mirror the situation with diffusible signals and their receptors, and imposes a cost on the speed and robustness of the interaction when there is no asymmetry [16]. There is also a need for experimental work to investigate these trade-offs.

Finally, mating-type-specific molecules can also be important for post-fusion events. Heterodimers of proteins specific to each of the mating partners are important for switching the mating programme off and initiating meiosis in several species. It has been argued that this function is itself key to the evolution of mating types [12,103]. For example, it allows cells to assess their ploidy level and so switch between vegetative growth, and gametic developmental programmes, and between mitosis and meiosis. From our perspective, this is but one of the factors that favour asymmetry.

4. Pairwise gamete interactions dictate the number of mating types

Let us now assume that the key role of mating types lies in securing an asymmetry in signalling interactions between gametes. We expect a proliferation of mating types as new rare types seldom meet themselves and so have an advantage over more common types (i.e. negative frequency dependence), leading to their spread until they reach a frequency equal to that of the residents [2,104]. This appears to describe the case in some ciliates and basidiomycetes that have very large numbers of mating types. However, most known isogamous species have only two mating types. Clearly, there must be some constraints that operate on gamete signalling limiting the evolutionary proliferation of mating types. We investigate this in a simple model that considers the strength of pairwise interactions between gametes and how this affects the spread and elimination of new types.

(a) Model outline

Consider a population with a single haploid locus M that defines the mating type, and assume n mating types are possible determined by alleles <m1, m2, … , mn>. We define the signalling preference of mating type i towards mating type j as pij and let pij take any positive value. This can be thought of as the ‘investment’ of mating type i in interactions with mating type j. Note, a more extensive treatment could be done by separating search, recognition and fusion functions, but for simplicity we consider these together, coded by a single locus. The mating probability between mating types i and j then depends on the product of their relative preferences for one another where .


Sexual selection

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Sexual selection, theory in postulating that the evolution of certain conspicuous physical traits—such as pronounced coloration, increased size, or striking adornments—in animals may grant the possessors of these traits greater success in obtaining mates. From the perspective of natural selection, such increases in mating opportunities outweigh the risks associated with the animal’s increased visibility in its environment. This concept was initially put forth by English naturalist Charles Darwin in The Descent of Man (1871).

Mutual attraction between the sexes is an important factor in reproduction. The males and females of many animal species are similar in size and shape except for the sexual organs and secondary sexual characteristics such as the breasts of female mammals. There are, however, species in which the sexes exhibit striking dimorphism (or physical difference). Particularly in birds and mammals, the males are often larger and stronger, more brightly coloured, or endowed with conspicuous ornamentation. These traits, however, make animals more visible to predators—the long plumage of male peacocks (Pavo cristatus) and birds of paradise (Paradisaea) and the enormous antlers of aged male deer (Odocoileus) are cumbersome loads in the best of cases. Darwin knew that natural selection could not be expected to favour the evolution of disadvantageous traits, and he was able to offer a solution to this problem. He proposed that such traits arise by “sexual selection,” which “depends not on a struggle for existence in relation to other organic beings or to external conditions but on a struggle between the individuals of one sex, generally the males, for the possession of the other sex.”

The concept of sexual selection as a special form of natural selection is easily explained. Other things being equal, organisms more proficient in securing mates have higher fitness. There are two general circumstances leading to sexual selection. One is the preference shown by one sex (often the females) for individuals of the other sex that exhibit certain traits. The other is increased strength (usually among the males) that yields greater success in securing mates.

The presence of a particular trait among the members of one sex can make them somehow more attractive to the opposite sex. This type of “sex appeal” has been experimentally demonstrated in all sorts of animals, from vinegar flies (Drosophila) to pigeons, mice, dogs (Canis lupus familiaris), and rhesus monkeys (Macacca mulatta). When, for example, Drosophila flies, some with yellow bodies as a result of spontaneous mutation and others with the normal yellowish gray pigmentation, are placed together, normal males are preferred over yellow males by females with either body colour.

Sexual selection can also come about because a trait—the antlers of a stag, for example—increases prowess in competition with members of the same sex. Stags, rams, and bulls use antlers or horns in contests of strength a winning male usually secures more female mates. Therefore, sexual selection may lead to increased size and aggressiveness in males. Male baboons (Papio) are more than twice as large as females, and the behaviour of the docile females contrasts with that of the aggressive males. A similar dimorphism occurs in the northern sea lion, Eumetopias jubata, where males weigh about 1,000 kg (2,200 pounds), about three times as much as females. The males fight fiercely in their competition for females large, battle-scarred males occupy their own rocky islets, each holding a harem of as many as 20 females. Among many mammals that live in packs, troops, or herds—such as wolves, horses, and buffaloes—there usually is a hierarchy of dominance based on age and strength, with males that rank high in the hierarchy doing most of the mating.


The evolution of plumage patterns in male and female birds

Waterfowl and gamebirds. Credit: Images via Wikimedia

(Phys.org) —Research published today looks at the evolutionary pathways to differences in bird plumage patterns between males and females – and concludes that birds are able to adapt their appearance with remarkable ease.

Ducks, geese and swans are waterfowl, an order known to scientists as Anseriformes. Hens, pheasants, partridges and turkeys are game-birds (Galliformes). Both orders are famous not just for their flesh but also for their striking and elaborate plumages which are sought after as decorative flourishes. Some members of these orders show marked differences in appearance between the sexes: a phenomenon known as sexual dimorphism. Male and female mallards look so different that for many years they were thought to be different species. In other members of the same orders, there is little apparent difference in the plumage of males and females.

Research by Cambridge PhD candidate Thanh-Lan Gluckman, published today in the Biological Journal of the Linnean Society, looks afresh at similarities and differences in plumage in almost 300 members of the Anseriformes and Galiformes orders – and focuses on patterning between male and female birds rather than colour. She said: "The colour of plumage has attracted much research interest, but the exquisite patterns of bird plumage, such as the spots of the guinea fowl and the barred patterns of ducks and turkeys, to just name a few, have received much less attention."

Since the 1980s, differences in the appearances of male and female birds have been seen through a prism of genetic correlation. In other words, it was thought that female birds may have evolved similar patterning to males due to common genes but that female patterns would be subsequently lost as it is not beneficial.

"It was argued that male birds developed their spectacular colours and elaborate patterning as a result of their mating patterns – they used their plumage to compete for and attract females. On the other hand, female birds needed to blend into their surroundings in order to nest safely and protect their young – so they became drab and dull to protect themselves and their young from predators," said Gluckman.

"My research looked at the plumage patterns of male and female birds on a separate and equal basis – and then went on to identify similarities and differences between them. By tracing the evolutionary pathways in the dimorphism of 288 species of waterfowl and gamebirds, I reconstructed the evolutionary history of plumage pattern sexual dimorphism, which allowed me to demonstrate that plumage patterns in females are not a result of genetic correlation. Essentially, what I found was that plumage patterning is remarkably labile – both male and female birds have the capacity to change between different types of patterns. What's interesting is to consider what are the forces driving these changes in male and female plumage patterns – whether they have an environmental basis and/or whether they have a signalling function between birds of different sexes or within the same sex."

As early as 1780, the Philosophical Transactions of the Royal Society of London published a paper by John Hunter proposing that plumage differences between the sexes were driven by sexual selection. Ever since, the prevailing view of sexual dimorphism has been one of showy males strutting their stuff to win over demure females. The predominant explanation put forward to explain how differences in dimorphism evolved hinges on mating habits males of polygamous species (those with more than one mate) had developed spectacular plumage in order to attract a maximum number of females, while monogamous species (those with one mate) retained similar plumage.

Gluckman said: "Previous research has shown that the traditional argument that differences in plumage between the sexes stem from differences in breeding systems doesn't always hold up. In many putatively monogamous species, the plumage of the males is significantly different to that of females and, likewise, males and females in many polygamous species have the same type of plumage. This suggests that plumage is not exclusively an outcome of breeding habits – but is a matter of function in a highly complex way."

In her study of patterning, Gluckman looked at the variations between the sexes of the same species and across species in order to build a picture of the pathways to similarity and differences between male and female bird plumage patterns. She used a classification of four broad types of patterning: mottled, scaled, barred and spotted. Birds exhibit a fabulous number of variations and combinations of these visual patterns in females as well as males.

"By emphasising similarities as well as differences in plumage patterns between male and female birds, rather than whether one sex is the same as the other, I found that sexual dimorphism in the plumage pattern of birds is highly nuanced and that there can be multiple types of sexual dimorphism. In expanding the definition of sexual dimorphism, and reconstructing evolutionary history, I found that changes in sexual dimorphism could be due to changes in males and/or females. In addition, the plumage patterns of birds seem to transition easily between different types of dimorphism, which is congruent with adaptation to fluctuating social and environmental conditions," said Gluckman.


Watch the video: The evolution of human mating: David Puts at TEDxPSU (January 2022).