Biology subjects

Constable, G. W. A.

Publications and source records attributed to Constable, G. W. A..

10 recordsLinked to original sources

bioRxiv2024

Estimating the rate of sexual reproduction and the inbreeding rate in Leishmania

Many eukaryotic species undergo sexual reproduction facultatively, either in response to stress or in particular environments. For the remainder of their life cycle they reproduce by mitosis. This facultative sex may be rare, which alters features of their evolutionary dynamics. Both the frequency of sex and the degree of inbreeding have been challenging to estimate from genome-scale polymorphism data. Here, we describe a method to estimate both these parameters based on the Moran model of heterozygous sites. We apply this method to population genomic data from Leishmania parasitic protozoans from the Leishmania donovani species complex, showing that these parasites undergo sexual reproduction approximately once per 10,000 generations and that populations vary considerably in the extent of their inbreeding.

genetics↗

bioRxiv2024

Cell size and selection for stress-induced binary cell fusion

In unicellular organisms, sexual reproduction typically begins with the fusion of two cells (plasmogamy) followed by the fusion of their two haploid nuclei (karyogamy) and finally meiosis. Most work on the evolution of sexual reproduction focuses on the benefits of the genetic recombination that takes place during meiosis. However, the selection pressures that may have driven the early evolution of binary cell fusion, which sets the stage for the evolution of karyogamy by bringing nuclei together in the same cell, have seen less attention. In this paper we develop a model for the coevolution of cell size and binary cell fusion rate. The model assumes that larger cells experience a survival advantage from their larger cytoplasmic volume. We find that under favourable environmental conditions, populations can evolve to produce larger cells that undergo obligate binary cell fission. However, under challenging environmental conditions, populations can evolve to subsequently produce smaller cells under binary cell fission that nevertheless retain a survival advantage by fusing with other cells. The model thus parsimoniously recaptures the empirical observation that sexual reproduction is typically triggered by adverse environmental conditions in many unicellular eukaryotes and draws conceptual links to the literature on the evolution of multicellularity. Author summarySexual reproduction is commonly observed, both in eukaryotic microorganisms and in higher multicellular organisms. Sex has evolved despite numerous apparent costs, including investment in finding a partner and the energetic requirements of sexual reproduction. Binary cell fusion is a process that sets the stage for sexual reproduction by bringing nuclei from different cells into contact. Here, we provide a mathematical explanation of the advantage conferred by binary cell fusion due to increased cell mass. We show that when unicellular organisms have the option to invest in either cell fusion or cell mass, they can evolve to fuse together as rapidly as possible in the face of adverse environments, instead of increasing their mass. These results are consistent with the empirical observation that sexual reproduction is often triggered by environmental stress in unicellular eukaryotes. Our results imply an advantage to cell fusion, which helps to shed light on the early evolution of sexual reproduction itself.

evolutionary biology↗

bioRxiv2023

Parthenogenesis, sexual conflict and the evolution of oogamy

In the face of varying environments, organisms exhibit a variety of reproductive modes, from asexuality to obligate sexuality. Should reproduction be sexual, the morphology of the sex cells (gametes) produced by these organisms has important evolutionary implications; these cells can be the same size (isogamy), one larger and one smaller (anisogamy), and finally the larger cell can lose its capacity for motility (oogamy, the familiar sperm-egg system). Understanding the origin of the sexes, which lies in the types of gametes they produce, thus amounts to explaining these evolutionary transitions. Here we extend classic results in this area by exploring these transitions in a model in which organisms can reproduce both sexually and asexually (a reproductive mode present in many algae). In particular, we investigate the co-evolution of gamete cell size with fertilization rate, which is a proxy for motility and pheromone production but usually held constant in such models. Using adaptive dynamics generalized to the case of switching environments, we find that isogamy can evolve to anisogamy through evolutionary branching, and that anisogamy can evolve to oogamy or suppressed pheromone production through a further branching driven by sexual conflict. We also derive analytic conditions on the model parameters required to arrest evolution on this isogamy-oogamy trajectory, with low fertilization rates and stochastically switching environments stabilizing isogamy under a bet-hedging strategy, and low fertilization costs stabilizing anisogamy and pheromone production.

evolutionary biology↗

bioRxiv2023

The evolution of parthenogen fertilization rates in switching environments: from facultative cell-fusion to oogamy

Organisms with external fertilisation exhibit a broad range of reproductive modes, from simple parthenogenesis to sexual reproduction encompassing isogamy, anisogamy, and oogamy, and including environmentally-mediated facultative sex. Here we develop a unifying mathematical model which explains the emergence of these modes via the coevolution of fertilization rate and cell size. Using a minimal assumption that survival is dependent on cell mass, and by carefully accounting for biological and evolutionary time scales, we find two distinct evolutionary outcomes: high fertilization rate (obligate sexuality) is selected when costs to cell fusion are low, while zero fertilization rate (obligate asexuality) is selected for when these costs are high. Surprisingy, in high fertilization rate scenarios evolving populations can transition from isogamy to anisogamy and oogamy via evolutionary branching. Furthermore, in variable environments we show that, without phenotypic plasticity, intermediate fertilization rates and isogamy can be maintained through bet-hedging. Allowing phenotypic plasticity can give rise to facultative sex; sexual reproduction in harsh environmental conditions, and asexuality in more benign conditions. These results parsimoniously explain a large range of empirically observed parthenogen reproduction strategies, and offer an hypothesis for the origin of binary cell fusion, a key step in the evolution of syngamy and sexual reproduction itself.

evolutionary biology↗

bioRxiv2022

Maternal transmission as a symbiont sieve, and the absence of lactation in male mammals

Gut microbiomes of humans carry a complex symbiotic assemblage of microorganisms. As in all mammals, the special mode of feeding newborn infants through milk from the mammary gland enhances the opportunity for vertical transmission of the milk microbiome from parents to the gut microbiome of offspring. This has potential benefits, but it also brings with it some hazards for the host. Here we use mathematical and numerical models to demonstrate that vertical transmission from both parents would allow host populations to be invaded by microbiome elements that are deleterious. In contrast, vertical transmission, when restricted to one parent, acts as a sieve preventing the spread of such elements. We show that deleterious symbionts generate selection for uniparental transmission in host populations, and that this selective advantage is maintained in the presence of moderate horizontal transmission. Some vertical transmission from mother to infant is bound to happen in placental mammals. This paper therefore puts forward the hypothesis that the asymmetry between females and males, together with the hazards that come with biparental transmission of the milk microbiome, generate selection against male lactation in humans, and in mammals in general.

evolutionary biology↗

bioRxiv2021

Parthenogenesis and the Evolution of Anisogamy

Recently, it was pointed out [1] that classic models for the evolution of anisogamy do not take into account the possibility of parthenogenetic reproduction, even though sex is facultative in many relevant taxa (e.g. algae) that harbour both anisogamous and isogamous species. Here we complement the analysis of [1] with an approach where we assume that the relationship between progeny size and its survival may differ between parthenogenetically and sexually produced progeny, favouring either the former or the latter. We show that the findings of [1], that parthenogenesis can stabilise isogamy relative to the obligate sex case, extend to our scenarios. We additionally investigate two different ways for one mating type to take over the entire population. First, parthenogenesis can lead to biased sex ratios that are sufficiently extreme that one type can displace the other, leading to de facto asexuality for the remaining type that now lacks partners to fuse with. This process involves positive feedback: microgametes, being numerous, lack opportunities for syngamy, and should they proliferate parthenogenetically, the next generation makes this asexual route even more prominent for microgametes. Second, we consider mutations to strict asexuality in producers of micro- or macrogametes, and show that the prospects of asexual invasion depend strongly on the mating type in which the mutation arises. Perhaps most interestingly, we also find scenarios in which parthenogens have an intrinsic survival advantage yet facultatively sexual isogamous populations are robust to the invasion of asexuals, despite us assuming no genetic benefits of recombination. Here equal contribution from both mating types to zygotes that are sufficiently well provisioned can outweigh the additional costs associated with syngamy.

evolutionary biology↗

bioRxiv2021

Genetic diversity in facultatively sexual populations and its implications for the origins of self-incompatibility in algae and fungi

The evolutionary mechanism that drove the establishment of self-incompatibility in early sexual eukaryotes is still a debated topic. While a number of competing hypotheses have been proposed, many have not received detailed theoretical attention. In particular, the hypothesis that self-incompatibility increases the benefits of genetic recombination in sexual haploids has been comparatively understudied. In this paper we address this topic by mathematically deriving how the probability of mating with a genetically distinct individual changes as a function of the presence or absence of self-incompatible mating type classes. We find that although populations with mating types successfully engage in sexual reproduction less frequently than their self-compatible competitors, they can nevertheless engage in useful sex with genetically distinct partners more frequently. This conclusion holds when the number of sexual reproductive events per generation is low (i.e. in small populations with low rates of facultative sexual reproduction). Finally we demonstrate the potential for frequency-dependent selection in competitive dynamics between self-compatible and self-incompatible types. These analytic results provide a baseline for studying the sex advantage enhancer model for the evolutionary origin of mating types within each specific hypothesis for the evolution of recombination. PACS87.23.-n Ecology and evolution, 87.23.Kg Dynamics of evolution, 02.50.Ey Stochastic processes 2000 MSC37N25: Dynamical systems in biology, 60J70: Applications of diffusion theory (population genetics, absorption problems, etc.)

evolutionary biology↗

bioRxiv2020

Switching environments, synchronous sex, and the evolution of mating types

While facultative sex is common in sexually reproducing species, for reasons of tractability most mathematical models assume that such sex is asynchronous in the population. In this paper, we develop a model of switching environments to instead capture the effect of an entire population transitioning synchronously between sexual and asexual modes of reproduction. We use this model to investigate the evolution of the number of self-incompatible mating types in finite populations, which empirically can range from two to thousands. When environmental switching is fast, we recover the results of earlier studies that implicitly assumed populations were engaged in asynchronous sexual reproduction. However when the environment switches slowly, we see deviations from previous asynchronous theory, including a lower number of mating types at equilibrium and bimodality in the stationary distribution of mating types. We provide analytic approximations for both the fast and slow switching regimes, as well as a numerical scheme based on the Kolmogorov equations for the system to quickly evaluate the model dynamics at intermediate parameters. Our approach exploits properties of integer partitions in number theory. We also demonstrate how additional biological processes such as selective sweeps can be accounted for in this switching environment framework, showing that beneficial mutations can further erode mating type diversity in synchronous facultatively sexual populations.

evolutionary biology↗

bioRxiv2019

Invasion and extinction dynamics of mating types under facultative sexual reproduction

In sexually reproducing isogamous species, syngamy between gametes is generally not indiscriminate, but rather restricted to occurring between complementary self-incompatible mating types. A longstanding question regards the evolutionary pressures that control the number of mating types observed in natural populations, which ranges from two to many thousands. Here, we describe a population genetic null model of this reproductive system and derive expressions for the stationary probability distribution of the number of mating types, the establishment probability of a newly arising mating type and the mean time to extinction of a resident type. Our results yield that the average rate of sexual reproduction in a population correlates positively with the expected number of mating types observed. We further show that the low number of mating types predicted in the rare-sex regime is primarily driven by low invasion probabilities of new mating type alleles, with established resident alleles being very stable over long evolutionary periods. Moreover, our model naturally exhibits varying selection strength dependent on the number of present mating types. This results in higher extinction and lower invasion rates for an increasing number of residents.

evolutionary biology↗

bioRxiv2017

Drift-Induced Selection Between Male And Female Heterogamety

Evolutionary transitions between male and female heterogamety are common in both vertebrates and invertebrates. Theoretical studies of these transitions have found that, when all genotypes are equally fit, continuous paths of intermediate equilibria link the two sex chromosome systems. This observation has led to a belief that neutral evolution along these paths can drive transitions, and that arbitrarily small fitness differences among sex chromosome genotypes can determine the system to which evolution leads. Here, we study stochastic evolutionary dynamics along these equilibrium paths. We find non-neutrality, both in transitions retaining the ancestral pair of sex chromosomes and in those creating a new pair. In fact, substitution rates are strongly biased in favor of dominant sex determining chromosomes, which fix with higher probabilities than mutations of no effect. Using diffusion approximations, we show that this non-neutrality is a result of drift-induced selection operating at every point along the equilibrium paths: stochastic jumps off the paths return, on average, with a directional bias in favor of the dominant segregating sex chromosome. Our results offer novel explanations for the ubiquity of transitions between male and female heterogamety and the preponderance of dominant major sex determining genes.

evolutionary biology↗