Sexual Reproduction In Animals Research Articles

Let's talk about sex: Why reproductive systems matter for understanding algae.

Sex is a crucial process that has molecular, genetic, cellular, organismal, and population-level consequences for eukaryotic evolution. Eukaryotic life cycles are composed of alternating haploid and diploid phases but are constrained by the need to accommodate the phenotypes of these different phases. Critical gaps in our understanding of evolutionary drivers of the diversity in algae life cycles include how selection acts to stabilize and change features of the life cycle. Moreover, most eukaryotes are partially clonal, engaging in both sexual and asexual reproduction. Yet, our understanding of the variation in their reproductive systems is largely based on sexual reproduction in animals or angiosperms. The relative balance of sexual versus asexual reproduction not only controls but also is in turn controlled by standing genetic variability, thereby shaping evolutionary trajectories. Thus, we must quantitatively assess the consequences of the variation in life cycles on reproductive systems. Algae are a polyphyletic group spread across many of the major eukaryotic lineages, providing powerful models by which to resolve this knowledge gap. There is, however, an alarming lack of data about the population genetics of most algae and, therefore, the relative frequency of sexual versus asexual processes. For many algae, the occurrence of sexual reproduction is unknown, observations have been lost in overlooked papers, or data on population genetics do not yet exist. This greatly restricts our ability to forecast the consequences of climate change on algal populations inhabiting terrestrial, aquatic, and marine ecosystems. This perspective summarizes our extant knowledge and provides some future directions to pursue broadly across micro- and macroalgal species.

Using individual-based modelling to investigate a pluralistic explanation for the prevalence of sexual reproduction in animal species

Attempts to resolve the paradox of sexual reproduction in animal species have typically involved single factor explanations, including but not limited to sexual species being better able to cope with fluctuating resources, being better able to evade pathogens and predators and sex facilitating the elimination of deleterious alleles. Only a handful of studies have investigated two potentially interacting factors, which most commonly involve the ability to evade pathogens and predators and mutation load; only two simulation studies by the same authors have examined the potential interaction of 3 factors.. Our study is the first three-factor study to examine the potential interaction between purifying selection, the ability to avoid predators and the ability to cope with fluctuating resources. Therefore, we addressed a number of open eco-evolutionary questions in our study: First, what is the effect of these three factors on the prevalence of sexual reproduction in animals? Second, do these factors act integratively, antagonistically or independently in determining the prevalence of sexual reproduction The ‘controls’ were our three prior studies where we investigated each of these factors individually. Our aim was to determine if the effect sizes in our individual studies were integratively enhanced by the interaction with the remaining two factors. What we found is that purifying selection purging deleterious alleles in sexual species was integratively enhanced by the two additional factors of increased predation and fluctuating resources. On the other hand, the effect of purifying selection and increased predation had an antagonistic effect on the levels of sexual reproduction and asexual reproduction in facultative species where there were fluctuating resources. Finally, the presence of an intermediate intensity deleterious allele and fluctuating resources had no discernable effect on the extinction levels of sexual and asexual species where there is increased predation. These results are not surprising, as there is no a priori reason to assume that multiple factors will have a greater impact on mode of reproduction than any of these factors acting independently. Our results suggest that multiple factors can act intergratively, antagonistically and non-reductively all at the same time, which is a significant contribution to the open question in the biological literature regarding the effect of multiple factors on the prevalence of sexual reproduction.

Characteristics of N6-methyladenosine Modification During Sexual Reproduction of Chlamydomonas reinhardtii

The unicellular green alga Chlamydomonas reinhardtii (hereafter Chlamydomonas) possesses both plant and animal attributes, and it is an ideal model organism for studying fundamental processes such as photosynthesis, sexual reproduction, and life cycle. N6-methyladenosine (m6A) is the most prevalent mRNA modification, and it plays important roles during sexual reproduction in animals and plants. However, the pattern and function of m6A modification during the sexual reproduction of Chlamydomonas remain unknown. Here, we performed transcriptome and methylated RNA immunoprecipitation sequencing (MeRIP-seq) analyses on six samples from different stages during sexual reproduction of the Chlamydomonas life cycle. The results show that m6A modification frequently occurs at the main motif of DRAC (D = G/A/U, R = A/G) in Chlamydomonas mRNAs. Moreover, m6A peaks in Chlamydomonas mRNAs are mainly enriched in the 3′ untranslated regions (3′UTRs) and negatively correlated with the abundance of transcripts at each stage. In particular, there is a significant negative correlation between the expression levels and the m6A levels of genes involved in the microtubule-associated pathway, indicating that m6A modification influences the sexual reproduction and the life cycle of Chlamydomonas by regulating microtubule-based movement. In summary, our findings are the first to demonstrate the distribution and the functions of m6A modification in Chlamydomonas mRNAs and provide new evolutionary insights into m6A modification in the process of sexual reproduction in other plant organisms.

Development of an in vitro tissue culture system for hammer coral (Fimbriaphyllia ancora) ovaries

In vitro gonad culture systems have proven useful to investigate intrinsic mechanisms of sexual reproduction in animals. Here we describe development of an in vitro culture method for coral ovaries. Mesenterial tissues containing both ovaries and mesenterial filaments were microscopically isolated from the scleractinian coral, Fimbriaphyllia ancora, and culture conditions were optimized. M199 diluted 10× (10% M199, pH 8.1) and supplemented with 25 mM HEPES and the antibiotics, ampicillin, penicillin and streptomycin, supported oocyte survival and maintained the structural integrity of ovaries during short-term culture (~ 6 days). Addition of a commercial antibiotic–antimycotic solution (Anti–Anti) and fetal bovine serum adversely affected ovary maintenance and caused tissue disintegration. Characterization of cultured ovaries showed that there is no difference in cell proliferation of ovarian somatic cells between culture Days 1 and 6. Moreover, the presence of oogonia and expression of a major yolk protein, vitellogenin, were confirmed in ovaries cultured for 6 days. This system will be useful for studying effects of a wide range of substances on coral oogenesis.

A Novel Spo11 Homologue Functions as a Positive Regulator in Cyst Differentiation in Giardia lamblia.

Giardia lamblia persists in a dormant state with a protective cyst wall for transmission. It is incompletely known how three cyst wall proteins (CWPs) are coordinately synthesized during encystation. Meiotic recombination is required for sexual reproduction in animals, fungi, and plants. It is initiated by formation of double-stranded breaks by a topoisomerase-like Spo11. It has been shown that exchange of genetic material in the fused nuclei occurs during Giardia encystation, suggesting parasexual recombination processes of this protozoan. Giardia possesses an evolutionarily conserved Spo11 with typical domains for cleavage reaction and an upregulated expression pattern during encystation. In this study, we asked whether Spo11 can activate encystation process, like other topoisomerases we previously characterized. We found that Spo11 was capable of binding to both single-stranded and double-stranded DNA in vitro and that it could also bind to the cwp promoters in vivo as accessed in chromatin immunoprecipitation assays. Spo11 interacted with WRKY and MYB2 (named from myeloblastosis), transcription factors that can activate cwp gene expression during encystation. Interestingly, overexpression of Spo11 resulted in increased expression of cwp1-3 and myb2 genes and cyst formation. Mutation of the Tyr residue for the active site or two conserved residues corresponding to key DNA-binding residues for Arabidopsis Spo11 reduced the levels of cwp1-3 and myb2 gene expression and cyst formation. Targeted disruption of spo11 gene with CRISPR/Cas9 system led to a significant decrease in cwp1-3 and myb2 gene expression and cyst number. Our results suggest that Spo11 acts as a positive regulator for Giardia differentiation into cyst.

Parthenogenetic vs. sexual reproduction in oribatid mite communities.

The dominance of sex in Metazoa is enigmatic. Sexual species allocate resources to the production of males, while potentially facing negative effects such as the loss of well‐adapted genotypes due to recombination, and exposure to diseases and predators during mating. Two major hypotheses have been put forward to explain the advantages of parthenogenetic versus sexual reproduction in animals, that is, the Red Queen hypothesis and the Tangled Bank/Structured Resource Theory of Sex. The Red Queen hypothesis assumes that antagonistic predator—prey/ parasite–host interactions favor sex. The Structured Resource Theory of Sex predicts sexual reproduction to be favored if resources are in short supply and aggregated in space. In soil, a remarkable number of invertebrates reproduce by parthenogenesis, and this pattern is most pronounced in oribatid mites (Oribatida, Acari). Oribatid mites are abundant in virtually any soil across very different habitats, and include many sexual and parthenogenetic (thelytokous) species. Thereby, they represent an ideal model group to investigate the role of sexual versus parthenogenetic reproduction across different ecosystems and habitats. Here, we compiled data on oribatid mite communities from different ecosystems and habitats across biomes, including tropical rainforests, temperate forests, grasslands, arable fields, salt marshes, bogs, caves, and deadwood. Based on the compiled dataset, we analyzed if the percentage of parthenogenetic species and the percentage of individuals of parthenogenetic species are related to total oribatid mite density, species number, and other potential driving factors of the reproductive mode including altitude and latitude. We then interpret the results in support of either the Red Queen hypothesis or the Structured Resource Theory of Sex. Overall, the data showed that low density of oribatid mites due to harsh environmental conditions is associated with high frequency of parthenogenesis supporting predictions of the Structured Resource Theory of Sex rather than the Red Queen hypothesis.

Nodal induces sequential restriction of germ cell factors during primordial germ cell specification.

Specification of the germ cell lineage is required for sexual reproduction in animals. The mechanism of germ cell specification varies among animals but roughly clusters into either inherited or inductive mechanisms. The inductive mechanism, the use of cell-cell interactions for germ cell specification, appears to be the ancestral mechanism in animal phylogeny, yet the pathways responsible for this process are only recently surfacing. Here, we show that germ cell factors in the sea star initially are present broadly, then become restricted dorsally and then in the left side of the embryo where the germ cells form a posterior enterocoel. We find that Nodal signaling is required for the restriction of two germ cell factors, Nanos and Vasa, during the early development of this animal. We learned that Nodal inhibits germ cell factor accumulation in three ways including: inhibition of specific transcription, degradation of specific mRNAs and inhibition of tissue morphogenesis. These results document a signaling mechanism required for the sequential restriction of germ cell factors, which causes a specific set of embryonic cells to become the primordial germ cells.

Sex-specific rejection in mate-guarding pair formation in the intertidal copepod, Tigriopus californicus.

Securing a potential mate is one of the most important processes in sexual reproduction of animals. Intertidal copepods of the genus Tigriopus show mate-guarding behavior where a male captures a female and continues to clasp her for up to two weeks prior to copulation. Although these copepods form a mate-guarding pair between a male and a female with high accuracy, interactions between the sexes in pair formation have not been well described and the mechanism allowing successful male-female pair formation is not yet understood. In this study, we performed experiments with Tigriopus californicus to analyze the behavior of both a capturer (male) and a captured individual (female or male) in formation of a guarding pair. While capturer males were attracted by both females and males, capture of virgin males was terminated in a significantly shorter time than that of virgin females. However, when presented freshly killed females or males, regardless of the sex of the body, capturer males continued to clasp the body for a comparable time as in an attempt on a living female. Our results suggest that a sex-specific rejection signal actively sent by captured males prevents male-male pair formation. Experiments also suggest that mated females reject an attempt of pair formation. To our knowledge, this is the first study to suggest involvement of active rejection by a captured individual in facilitation of reproductively successful male-female guarding pair formation in the genus Tigriopus.

Abscisic acid controlled sex before transpiration in vascular plants

Sexual reproduction in animals and plants shares common elements, including sperm and egg production, but unlike animals, little is known about the regulatory pathways that determine the sex of plants. Here we use mutants and gene silencing in a fern species to identify a core regulatory mechanism in plant sexual differentiation. A key player in fern sex differentiation is the phytohormone abscisic acid (ABA), which regulates the sex ratio of male to hermaphrodite tissues during the reproductive cycle. Our analysis shows that in the fern Ceratopteris richardii, a gene homologous to core ABA transduction genes in flowering plants [SNF1-related kinase2s (SnRK2s)] is primarily responsible for the hormonal control of sex determination. Furthermore, we provide evidence that this ABA-SnRK2 signaling pathway has transitioned from determining the sex of ferns to controlling seed dormancy in the earliest seed plants before being co-opted to control transpiration and CO2 exchange in derived seed plants. By tracing the evolutionary history of this ABA signaling pathway from plant reproduction through to its role in the global regulation of plant-atmosphere gas exchange during the last 450 million years, we highlight the extraordinary effect of the ABA-SnRK2 signaling pathway in plant evolution and vegetation function.

Membrane-Bound RLCKs LIP1 and LIP2 Are Essential Male Factors Controlling Male-Female Attraction in Arabidopsis

Successful sexual reproduction in animals and plants requires communication between male and female gametes. In flowering plants, unlike in animals, eggs and sperm cells are enclosed in multicellular embryo sacs and pollen grains, respectively; guided growth of the pollen tube into the ovule is necessary for fertilization. Pollen tube guidance requires accurate perception of ovule-emitted guidance cues by the receptors in pollen tubes. Although several ovule-secreted peptides controlling pollen tube guidance have recently been identified, i.e., maize EGG APPARATUS1 (EA1), Torenia LURE1/LURE2, and Arabidopsis CRP810_1/AtLURE1, little is known about the receptors. Here, we identified two receptor-like kinase (RLK) genes preferentially expressed in Arabidopsis pollen tubes, Lost In Pollen tube guidance 1 (LIP1) and 2 (LIP2), which are involved in guidance control of pollen tubes. LIP1 and LIP2 were anchored to the membrane in the pollen tube tip region via palmitoylation, which was essential for their guidance control. Simultaneous inactivation of LIP1 and LIP2 led to impaired pollen tube guidance into micropyle and significantly reduced attraction of pollen tubes toward AtLURE1. Our results suggest that LIP1 and LIP2 represent essential components of the pollen tube receptor complex to perceive the female signal AtLURE1 for micropylar pollen tube guidance.

BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana

Nuclear fusion is an essential process in the sexual reproduction of animals and plants. In flowering plants, nuclear fusion occurs three times: once during female gametogenesis, when the two polar nuclei fuse to produce the diploid central cell nucleus, and twice during double fertilization. The yeast Ig binding protein (BiP) is a molecular chaperone Hsp70 in the endoplasmic reticulum that regulates nuclear membrane fusion during mating. Here we report that in Arabidopsis thaliana, BiP is involved in the fusion of polar nuclei during female gametophyte development. BiP-deficient mature female gametophytes contain two unfused polar nuclei, in spite of their close contact. This indicates a surprising conservation of BiP function in nuclear fusion between plants and yeasts. We also found that endosperm nuclear division becomes aberrant after fertilization of the BiP-deficient female gametophytes with wild-type pollen. This is experimental evidence for the importance of fusion of the polar nuclei in the proliferation of endosperm nuclei.

Gαo/i and Gαs Signaling Function in Parallel with the MSP/Eph Receptor to Control Meiotic Diapause in C. elegans

A conserved biological feature of sexual reproduction in animals is that oocytes arrest in meiotic prophase and resume meiosis in response to extraovarian signals. In C. elegans, sperm trigger meiotic resumption by means of the major sperm protein (MSP) signal. MSP promotes meiotic resumption by functioning as an ephrin-signaling antagonist and by counteracting inhibitory inputs from the somatic gonadal sheath cells. By using a genome-wide RNAi screen in a female-sterile genetic background, we identified 17 conserved genes that maintain meiotic arrest in the absence of the MSP signal. In vitro binding experiments show that MSP promotes oocyte mitogen-activated protein kinase activation and meiotic maturation in part through direct interaction with the VAB-1 Eph receptor. Four conserved proteins, including a disabled protein (DAB-1), a vav family GEF (VAV-1), a protein kinase C (PKC-1), and a STAM homolog (PQN-19), function with the VAB-1 Eph/MSP receptor in oocytes. We show that antagonistic Galphao/i and Galphas signaling pathways function in the soma to regulate meiotic maturation in parallel to the VAB-1 pathway. Galphas activity is necessary and sufficient to promote meiotic maturation, which it does in part by antagonizing inhibitory sheath/oocyte gap-junctional communication. Our findings show that oocyte Eph receptor and somatic cell G protein signaling pathways control meiotic diapause in C. elegans, highlighting contrasts and parallels between MSP signaling in C. elegans and luteinizing hormone signaling in mammals.

Regulation of Sperm Activation by SWM-1 Is Required for Reproductive Success of C. elegans Males

Sexual reproduction in animals requires the production of highly specialized motile sperm cells that can navigate to and fertilize ova. During sperm differentiation, nonmotile spermatids are remodeled into motile spermatozoa through a process known as spermiogenesis. In nematodes, spermiogenesis, or sperm activation, involves a rapid cellular morphogenesis that converts unpolarized round spermatids into polarized amoeboid spermatozoa capable of both motility and fertilization. Here we demonstrate, by genetic analysis and in vivo and in vitro cell-based assays, that the temporal and spatial localization of spermiogenesis are critical determinants of male fertility in C. elegans, a male/hermaphrodite species. We identify swm-1 as a factor important for male but not hermaphrodite fertility. We show that whereas in wild-type males, activation occurs after spermatids are transferred to the hermaphrodite, swm-1 mutants exhibit ectopic activation of sperm within the male reproductive tract. This ectopic activation leads to infertility by impeding sperm transfer. The SWM-1 protein is composed of a signal sequence and two trypsin inhibitor-like domains and likely functions as a secreted serine protease inhibitor that targets two distinct proteases. These findings support a model in which (1) proteolysis acts as an important in vivo trigger for sperm activation and (2) regulating the timing of proteolysis-triggered activation is crucial for male reproductive success. Furthermore, our data provide insight into how a common program of gamete differentiation can be modulated to allow males to participate in reproduction in the context of a male/hermaphrodite species where the capacity for hermaphrodite self-fertilization has rendered them nonessential for progeny production.

Evolution of Sexuality: Biology and Behavior

Sexual reproduction in animals and plants is far more prevalent than asexual reproduction, and there is no dearth of hypotheses attempting to explain why. Even bacteria and viruses, which reproduce by cloning, engage in promiscuous horizontal gene exchange (“parasexual reproduction”) on such short time scales that they evolve genotypic diversity even more rapidly than eukaryotes. (We confront this daily in the form of antimicrobial resistance.) The host-parasite and host-pathogen arms race purports to explain the prevalence of sexual reproduction, yet there are over a dozen other hypotheses, including the proposition that sexual reproduction purges the genome of deleterious mutations. An equally daunting challenge is to understand, in terms of evolutionary logic, the jungle of diverse courtship and mating strategies that we find in nature. The phenotypic plasticity of sex determination in animals suggests that the central nervous system and reproductive tract may not reach the same endpoint on the continuum between our stereotypic male and female extremes. Why are there only two kinds of gametes in most eukaryotes? Why are most flowering plants, and few animals, hermaphroditic? Why do male animals compete more for access to females than the other way around in most animals that have been studied? This review presents more questions than answers, but an extraordinary wealth of data has been collected, and new genetic techniques will provide new answers. The possible relevance of these data to human sexuality will be discussed in a future article.

Swifter, Higher, Stronger

ECOLOGY/EVOLUTION Sexual selection, the evolutionary corollary of mate choice, is generally studied in organisms where direct matings (for example, internal fertilization) between individuals take place. The variance in male mating success that results when females choose, in particular, can lead to the evolution of showy and sometimes bizarre signals of male quality. However, the ancestral condition for sexual reproduction in animals is broadcast spawning and external fertilization—that is, the release of sperm and eggs by benthic marine organisms into the water column. Does sexual selection operate under these conditions? In an experimental study of reproduction in sea urchins, Levitan finds that sexual selection—as identified by the difference between males and females in the variance for fertilization success—does indeed occur, but only at intermediate population densities of males and females. At low and high densities, the variance in fertilization success did not differ between the sexes, because of sperm limitation at low density and sperm competition at high density. Hence, sexual selection in sea urchins is under control of the adult only in the sense of timing and quantity of gamete release; the rest is mediated by traits of the gametes themselves. — AMS Am. Nat. 164 , 298 (2004).

Sex and Parthenogenesis in Sparse Populations

A model is developed to predict the minimum population density required (critical density) for successful sexual reproduction in animals. The model predicts that: (1) Hermaphroditic reproduction requires only half the critical density of bisexual reproduction; (2) a linear increase in mortality results in an exponential increase in critical density; and (3) increasing the time interval between clutches reduces critical density but makes a population more sensitive to external mortality. The probability of encountering a mate is dependent on the distance at which a male can detect a female. If predators can also detect females, there is an optimum conspicuousness for a female, which is dependent on the densities of males and of predators. A female should be very conspicuous only when both predators and males are rare. In an application of the model to zooplankton species, the smallest zooplankters are predicted to require relatively high densities for sexual reproduction. These animals reproduce with cycli...