Anisogamous Species Research Articles

Unraveling the mating system of the burrowing shrimp Lepidophthalmus siriboia (Decapoda Callichiridae) based on life history traits

Natural history studies are important in helping to understand the origin and evolution of social organization as well as the evolution of specialized morphological structures linked to mating behavior of animals. Here we describe the burrow use pattern, sex ratio, and sexual dimorphism of the burrowing shrimp Lepidophthalmus siriboia to test a series of evolutionary hypotheses. To this end, a total of 259 individuals of L. siriboia were collected from the northeast region of Brazil. No shrimp pairs or burrows inhabited by more than one shrimp were detected during the study period. A solitary habit is a non-random behavior in this species because single shrimps were found with a greater frequency than expected by chance. All ovigerous females were found living solitarily, which suggests that males abandon these females shortly after insemination. Contrary to the expectations of an anisogamous species, L. siriboia produced a female-biased operational sex ratio (OSR), contradicting the hypothesis that only males compete for mates. The latter was supported by the existence of sexual dimorphism in cheliped size, a condition that argues in favor of female–female competition in this species. In the same line of reasoning, heterochely was present in adult males, although it was also present to a lesser degree in adult females. Female asymmetry of chelipeds suggests the evolution of an unconventional role in female major cheliped use. The major cheliped showed a positive allometric growth pattern through the ontogeny of both sexes. However, when growth patterns of the major and minor chelipeds were compared, the fitted regression lines for each sex had different slopes, indicating that the cheliped could be an appendage sexually selected by individuals of the opposite sex during mating.

Sexual selection in seaweed? Testing Bateman's principles in the red alga Gracilaria gracilis.

In anisogamous species, sexual selection is expected to be stronger in males. Bateman's principles state that the variance in (i) reproductive and (ii) mating success is greater for males, and (iii) the relationship between reproductive success and mating success (the Bateman gradient) is also stronger for males than for females. Sexual selection, based on Bateman's principles, has been demonstrated in animals and some angiosperms, but never in a seaweed. Here we focus on the oogamous haploid-diploid rhodophyte Gracilaria gracilis in which previous studies have shown evidence for non-random mating, suggesting the existence of male-male competition and female choice. We estimated mating and reproductive success using paternity analyses in a natural population where up to 92% of fertilizations occurred between partners of that population. The results show that the variance in mating success is significantly greater in males than in females and that the Bateman gradient is positive only in males. Distance to female partners also explains a minor part of the variance in male mating success. Although there is no evidence for sexual dimorphism, our study supports the hypothesis that sexual selection occurs in G. gracilis, probably on male traits, even if we cannot observe, characterize or quantify them yet.

Sex Without Sexes: Can the Cost of Finding a Mate Explain Diversity in Fungal Mating Systems?

Eukaryotes have evolved myriad ways of uniting gametes during sexual reproduction. A repeated pattern is the convergent evolution of a mating system with the fusion of larger gametes with smaller gametes (anisogamy) from that of fusion between morphologically identical gametes (isogamy). In anisogamous species, sexes are defined as individuals that produce only one gamete type. Although sexes abound throughout Eukarya, in fungi there are no biological sexes, because even in anisogamous species, individuals are hermaphroditic and produce both gamete types. For this reason, the term mating types is preferred over sexes, and, thus defined, only individuals of differing mating types can mate (homoallelic incompatibility). In anisogamous fungal species, there is scant evidence that there are more than two mating types, and this may be linked to genetic constraints, such as the use of mating types to determine the inheritance of cytoplasmic genomes. However, the mushroom fungi (Agaricomycetes) stand out as having both large numbers of mating types within a species, which will allow nearly all individuals to be compatible with each other, and reciprocal exchange of nuclei during mating, which will avoid cytoplasmic mixing and cyto-nuclear conflicts. Although the limitation of mating types to two in most fungi is consistent with the cyto-nuclear conflicts model, there are many facets of the Agaricomycete life cycle that also suggest they will demand a high outbreeding efficiency. Specifically, they are mostly obligately sexual and outcrossing, inhabit complex competitive niches, and display broadcast spore dispersal. Subsequently, the Agaricomycete individual pays a high cost to being choosy when encountering a mate. Here, I discuss the costs of mate finding and choice and demonstrate how most fungi have multiple ways of reducing these costs, which can explain why mating types are mostly limited to two per species. Nevertheless, it is perplexing that fungi have not evolved multiple mating types on more occasions nor evolved sexes. The few exceptions to these rules suggest that it is dictated by both molecular and evolutionary constraints.

Sex-specific Positioning of the Mating Structure in Scale-bearing Gametes of Monostroma angicava and Collinsiella cava (Ulvophyceae, Chlorophyta): A Possible Widespread Difference between Male and Female Gametes.

The gametes of chlorophytes can be divided into two morphological types (types α and β) based on the position of the mating structure relative to the flagella and eyespot. To elucidate the relationship between the morphological types and the sexes, we studied spatial relationships between the flagellar apparatus-eyespot-mating structures in biflagellate male and female gametes and their fate after fertilization in the anisogamous (Monostroma angicava) and the slightly anisogamous species (Collinsiella cava) using field emission scanning electron microscopy and transmission electron microscopy. The smaller male and larger female gametes of M. angicava had two basal bodies arranged at a 180° angle and the cell surface coated with square-shaped body scales, except for the flagella and mating structures. The mating structure of the female gamete was located on the same side of the flagellar beat plane as the eyespot (type β), whereas that of the male gamete was located on the opposite side (type α). This mating structure arrangement was also confirmed in C. cava. The initial fusion when male and female gametes were mixed involved the mating structures. In a fusing pair of gametes, each flagellum of one gamete lay alongside one flagellum of the other gamete. As fusion proceeded, the gamete pair transformed into a quadriflagellate planozygote, in which the four basal bodies were arranged in a cruciate pattern. The eyespots were positioned side-by-side on the same side of the cell. These results suggest that the two morphological types of gametes are intimately correlated with the particular sexes.

Flagellar motility during sperm chemotaxis and phototaxis in fucalean algae

ABSTRACT The swimming of male gametes of brown algae is controlled by two heterokont flagella, regardless of reproductive system, but the patterns of flagellar movement can vary. We investigated sperm chemotaxis and phototaxis in four oogamous Australasian fucalean species. Sperm morphology was similar to that of male gametes of isogamous and anisogamous species but their chemotactic behaviours were much closer to those of other oogamous species than those of isogamous and anisogamous species. Moreover, unlike anisogamous species, sperm chemotaxis of the oogamous species, Hormosira banksii, was not inhibited by a phosphodiesterase inhibitor, theophylline, suggesting variability in regulatory mechanisms of sperm chemotaxis amongst brown algae. In our previous work, lower extracellular Ca2+, supernatant of female gametes and theophylline induced the reversal of phototactic signs in anisogamous male gametes. In contrast, lower extracellular Ca2+ and theophylline did not significantly affect phototaxis in sperm of the oogamous H. banksii. Moreover, high extracellular Ca2+ and supernatant of eggs disrupted the negative phototaxis but did not reverse their phototactic sign. These results suggest that the regulation of phototaxis also varies amongst brown algal gametes. Further investigation of brown algal species is warranted to assess the generality of these patterns of chemotaxis and phototaxis among anisogamous and oogamous gametes.

Isogamy in large and complex volvocine algae is consistent with the gamete competition theory of the evolution of anisogamy.

Although the gamete competition theory remains the dominant explanation for the evolution of anisogamy, well-known exceptions to its predictions have raised doubts about the completeness of the theory. One of these exceptions is isogamy in large or complex species of green algae. Here, we show that this exception may be explained in a manner consistent with a game-theoretic extension of the original theory: a constraint on the minimum size of a gamete may prevent the evolution of continuously stable anisogamy. We show that in the volvocine algae, both gametes of isogamous species retain an intact chloroplast, whereas the chloroplast of the microgamete in anisogamous species is invariably degenerate. The chloroplast, which functions in photosynthesis and starch storage, may be necessary to provision a gamete for an extended period when gamete encounter rates are low. The single chloroplast accounts for most of the volume of a typical gamete, and thus may constrain the minimum size of a gamete, preventing the evolution of anisogamy. A prediction from this hypothesis, that isogametes should be larger than the microgametes of similar-size species, is confirmed for the volvocine algae. Our results support the gamete competition theory.

Evolutionary divergence of the sex-determining gene MID uncoupled from the transition to anisogamy in volvocine algae.

Volvocine algae constitute a unique comparative model for investigating the evolution of oogamy from isogamous mating types. The sex- or mating type-determining gene MID encodes a conserved RWP-RK transcription factor found in either the MT- or male mating locus of dioecious volvocine species. We previously found that MID from the isogamous species Chlamydomonas reinhardtii (CrMID) could not induce ectopic spermatogenesis when expressed heterologously in Volvox carteri females, suggesting coevolution of Mid function with gamete dimorphism. Here we found that ectopic expression of MID from the anisogamous species Pleodorina starrii (PsMID) could efficiently induce spermatogenesis when expressed in V. carteri females and, unexpectedly, that GpMID from the isogamous species Gonium pectorale was also able to induce V. carteri spermatogenesis. Neither VcMID nor GpMID could complement a C. reinhardtii mid mutant, at least partly owing to instability of heterologous Mid proteins. Our data show that Mid divergence was not a major contributor to the transition between isogamy and anisogamy/oogamy in volvocine algae, and instead implicate changes in cis-regulatory interactions and/or trans-acting factors of the Mid network in the evolution of sexual dimorphism.

The evolution of sexes: A specific test of the disruptive selection theory.

The disruptive selection theory of the evolution of anisogamy posits that the evolution of a larger body or greater organismal complexity selects for a larger zygote, which in turn selects for larger gametes. This may provide the opportunity for one mating type to produce more numerous, small gametes, forcing the other mating type to produce fewer, large gametes. Predictions common to this and related theories have been partially upheld. Here, a prediction specific to the disruptive selection theory is derived from a previously published game‐theoretic model that represents the most complete description of the theory. The prediction, that the ratio of macrogamete to microgamete size should be above three for anisogamous species, is supported for the volvocine algae. A fully population genetic implementation of the model, involving mutation, genetic drift, and selection, is used to verify the game‐theoretic approach and accurately simulates the evolution of gamete sizes in anisogamous species. This model was extended to include a locus for gamete motility and shows that oogamy should evolve whenever there is costly motility. The classic twofold cost of sex may be derived from the fitness functions of these models, showing that this cost is ultimately due to genetic conflict.

Population sex ratio and dispersal in experimental, two‐patch metapopulations of butterflies

1. Sex-biased dispersal, that is, the difference in dispersal between males and females, is thought to be the consequence of any divergent evolutionary responses between sexes. In anisogamous species, asymmetry in parental investment may lead to sexual conflict, which entails male-male competition (for sexual partner access), female-female competition (for feeding or egg-laying habitat patches) and/or male-female competition (antagonistic co-evolution). 2. As competition is one of the main causes of dispersal evolution, intra- and intersexual competition should have strong consequences on sex-biased dispersal. However, very few experimental studies, if any, have simultaneously addressed the effect of biased sex ratio on (i) each dispersal stage (emigration, transience, immigration), (ii) the dispersal phenotype and (iii) the colonization success of new habitat in order to fully separate the effects of varying male and female density. 3. Here, we used the Metatron, a unique experimental system composed of 48 interconnected enclosed patches dedicated to the study of dispersal in meta-ecosystems, to investigate the effect of sex ratio on dispersal in a butterfly. We created six populations with three different sex ratios in pairs of patches and recorded individual movements in these simple metapopulations. 4. Emigration was higher when the proportion of males was higher, and individuals reached the empty patch at a higher rate when the sex ratio in the departure patch was balanced. Males had a better dispersal success than females, which had a lower survival rate during dispersal and after colonization. We also showed that sex and wing size are major components of the dispersal response. 5. We did not observe sex-biased dispersal; our results thus suggest that female harassment by males and male-male competition might be more important mechanisms for the dispersal of females and males, than the search for a mating partner. Furthermore, the demonstration of a differential mortality between males and females during dispersal provides causal hypotheses of the evolution of sex-biased dispersal.

Underwater fertilization dynamics of marine green algae

We studied the fertilization dynamics of marine green algae with both analytical methods and numerical simulations. In this study, we focused on a new factor, gametic investment per unit volume of the space in which gametes searched for their partners, and compared the numbers of zygotes formed at lower investments with those at higher investments. As a function of the gametic investment for various anisogamy ratios, we found there was generally a crossover region for each series where, for gametic investments larger than the crossover region, isogamy prevailed with the highest number of zygotes formed, while for gametic investments smaller than the crossover region, anisogamy dominated. These results may explain both the stable maintenance of isogamy in shallow water and the distribution of anisogamous species in deep water, since in shallow water the gametic investments typically exceed this crossover region and vice versa. Comparisons of field data from marine green algae are consistent with this hypothesis. Also, we showed that the cost of sex was approximately twofold in zygote formation when comparing isogamous species with mating types to those without mating types.

Simulation of gamete behaviors and the evolution of anisogamy: reproductive strategies of marine green algae

In marine green algae, isogamous or slightly anisogamous species are taxonomically widespread. They produce positively phototactic gametes in both sexes. We developed a new numerical simulator of gamete behavior using C++ and pseudo‐parallelization methods to elucidate potential advantages of phototaxis. Input parameters were set based on experimental data. Each gamete swimming in a virtual rectangular test tank was tracked and the distances between the centers of nearby male and female were measured at each step to detect collisions. Our results shed light on the roles of gamete behavior and the mechanisms of the evolution of anisogamy and more derived forms of sexual dimorphism. We demonstrated that not only gametes with positive phototaxis were favored over those without, particularly in shallow water. This was because they could search for potential mates on the 2‐D water surface rather than randomly in three dimensions. Also, phototactic behavior clarified the difference between isogamy and slight anisogamy. Isogamous species produced more zygotes than slightly anisogamous ones only under the phototactic conditions. Our results suggested that ‘sperm limitation’ might be easily resolved particularly in the slightly anisogamous species. Some more markedly anisogamous species produce the smaller male gametes without any phototactic devices and the larger positively phototactic female gametes. In such species, female gametes attract their partners using a sexual pheromone. This pheromonal attraction system might have played a key role in the evolution of anisogamy, because it could enable markedly anisogamous species achieve 2‐D search efficiencies on the water surface. The mating systems appear to be tightly tuned o the environmental conditions of their habitats.

Phototaxis and the evolution of isogamy and ‘slight anisogamy’ in marine green algae: insights from laboratory observations and numerical experiments

The evolution of anisogamy in marine algae was studied through numerical simulations of gamete mating behaviour in three dimensions, using observed traits of marine green algae as input parameters. The importance of phototaxis became apparent from the numerical experiments: all gametes with phototactic systems are favoured over those without, but this advantage is reduced with increasing tank depth or shorter search times. Phototactic gametes were advantaged over non-phototactic gametes if the water was shallower than about 30–40 mm when the time available for gamete encounter was 1000 time steps (5.55 min). If gametes of both sexes are positively phototactic, slightly anisogamous species are at a disadvantage to isogamous species, which invalidates the sperm-limitation theory as a driver for the evolution of slight anisogamy. Conflicting selection forces of search efficiency and zygote fitness may be needed. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 144, 321–327.

The costs of sex due to deleterious intracellular parasites

Abstract A major problem in evolutionary theory is to explain the widespread occurrence of sexual recombination. This is particularly difficult in anisogamous species where the familiar ‘two-fold cost of sex’ is encountered. Another cost has recently been identified: that fusion of gametes allows intracellular parasites or deleterious ‘selfish’ genomes to invade a population. These costs of anisogamy and the ability of cytoplasmic agents to invade a sexual population are quantified, allowing the costs and consequences of different modes of reproduction to be compared. It is found that the costs of selfish elements are likely to be very high and, in particular, that isogamous sexual reproduction (the putative ‘primitive’ form) is not cost-free, but incurs a fitness reduction of the order of 90%; thus a large selective disadvantage occurs in the initial evolution of sex which is ignored in standard analysis. Even once anisogamy has evolved, the low levels of ‘paternal leakage’ observed in many extant organisms may allow selfish cytoplasmic elements to spread, resulting in moderate to large decreases in host population fitness. However, much of the cost of selfish elements is avoided in sexual lifecycles with a large number of asexual cellular divisions between sexual reproduction: this greatly impedes the spread of selfish agents and reduces the fitness loss attributable to selfish elements.

Evolution of the alternation of haploid and diploid phases in life cycles. II. Maintenance of the haplo‐diplontic cycle

AbstractThe relative duration of the haploid and the diploid phases during the reproductive cycle varies greatly between organisms. This paper addresses the question of the evolution of haploid, diploid, and haplo‐diplontic life cycles. When the life span of haploid and diploid individuals is constant whatever their cycle, we show that the haplo‐diplontic cycle has an advantage, which depends on the sex‐ratio in anisogamous species and on the probability of fertilization in isogamous species. This is because meiosis and fertilization occur half as often in the haplo‐diplontic cycle as in haploid or diploid cycles, for the same number of generations of individuals. This argument is demonstrated using a model which considers a genetic determination of the cycle, and fixed haploid and diploid fitnesses. The relevance of measures of fitness of haploid and diploid individuals in predicting the evolution of life cycles is discussed. Measures obtained in algae are compared with theoretical predictions.

Evolution of gamete motility differences II. Interaction with the evolution of anisogamy

In this paper the population genetic analysis of the evolution of a gamete motility dimorphism is carried further. In contrast to the preceding paper ( Hoekstra, Janz & Schilstra, 1984 ) the existence of two mating types (based on pheromonal gamete attraction) is assumed. This broadens the conditions for a stable gamete motility dimorphism, provided there is initially some linkage between the loci for gamete motility and pheromone production/response. The effect of anisogamy on gamete motility is added to the assumptions of Parker, Baker & Smith (1972) for the evolution of anisogamy; this appeared to broaden the conditions for stable anisogamy only when the loci for gamete size and for mating type are closely linked. However, anisogamy can also evolve solely as a consequence of its effect on gamete motility, provided the size difference between the gamete types is sufficiently large. This alternative explanation of the evolution of anisogamy is corroborated by the fact that pheromonal gamete attraction mechanisms are generally absent in isogamous species but present in anisogamous species.