Biology subjects

Pomiankowski, A.

Publications and source records attributed to Pomiankowski, A..

17 recordsLinked to original sources

bioRxiv2025

First growth, then information: the path to genetic heredity in protocells

Most theoretical work on the origin of heredity has focused on how genetic information can be maintained without mutational degradation in the absence of error-proofing systems. A simple and parsimonious solution assumes the first gene sequences evolved inside dividing protocells, which enables selection for functional sets. But these models of information maintenance do not consider how protocells acquired their genetic information in the first place. Clues to this transition are suggested by patterns in the genetic code, which indicate a strong link to autotrophic metabolism, with early translation based on direct physical interactions between amino acids and short RNA polymers, grounded in their hydrophobicity. Here, we develop a mathematical model to investigate how random RNA polymers inside autotrophically growing protocells could evolve better coding sequences for discrete functions. The model tracks a population of protocells that evolve towards two essential functions: CO2 fixation (which drives monomer synthesis and cell growth) and copying (which amplifies replication and translation of sequences inside protocells). The model shows that distinct coding sequences can emerge from random RNA sequences driving increased protocell division. The analysis reveals an important restriction: growth-supporting functions such as CO2 fixation must be more easily attained than informational processes such as RNA copying and translation. This uncovers a fundamental constraint on the emergence of genetic heredity: growth precedes information at the origin of life.

evolutionary biology↗

bioRxiv2025

Dynamic evolution of germ-line restricted chromosomes in three dark-winged fungus gnats (Sciaridae) revealed through chromosome level germline genomes.

Germline restricted chromosomes (GRCs) are an evolutionary mystery. While they seem to be important and perhaps indispensable in species they occur, they also show surprising variability in copy number and size. We are just beginning to understand the evolutionary significance of these chromosomes. One factor that impedes our understanding is that at present, few clades with these chromosomes have been studied in depth. We genomically investigate the GRCs in dark-winged fungus gnats (Sciaridae), a cosmopolitan and species-rich taxa which have harboured GRCs for at least 58 million years. Sciaridae species carry from 1-4 large GRCs which evolved through introgression from the Cecidomyiidae lineage. We produce the first male germline chromosome-scale genome assemblies for the sciarids Bradysia coprophila, B. impatiens, and Lycoriella ingenua. Comparing the GRCs both between and within species, we find that these chromosomes evolve in an extraordinarily dynamic fashion, with very little conservation of synteny or gene content. Puzzlingly, despite this variability, GRCs are gene rich and their genes are evolving under strong purifying selection. Additionally, we uncover evidence that somatic elimination of GRCs potentially occurs via a satellite mediated process. Our study sheds light on the mechanisms of meiosis, tissue restriction, chromosome elimination, and gives us a better appreciation for the diversity of genetic systems that not only persist, but thrive in nature. Significance statementGermline restricted chromosomes (GRCs) are a fascinating evolutionary puzzle. They are restricted to the germline early in development, have unusual transmission dynamics and are more variable than core chromosomes, but also seem to be indispensable in clades they occur in. We generate chromosome level GRC assemblies from three species of fungus gnats (Sciaridae, Diptera). We find that the GRCs, which originated via a cross-family hybridization event, are evolving much more dynamically than other chromosomes in the genome. The five GRCs we sequence are all large, gene-rich, and seem to carry functional genes, but contain mostly a non-overlapping gene set, suggesting that four of the five GRCs we sequenced did not evolve from the same original chromosome.

evolutionary biology↗

bioRxiv2025

Eukaryotic recombinases duplicated after divergence from known asgardarchaeal RadA: implications for the evolution of sex during eukaryogenesis

The origin of meiotic sex was a key milestone in the evolution of the eukaryotic cell. The DNA recombinases Rad51 and DMC1 have been used previously to trace the timing and origins of the meiotic machinery, and warrant revisiting in the face of the recent increased diversity of reported asgardarchaeal taxa. Here we perform comparative genomics and phylogenetic analyses of RadA protein sequences from a broad sampling of eukaryotic and archaeal taxa. We show that even with increased and new sampling, the eukaryotic Rad51 and DMC1 proteins still resolve separately from any archaeal RadA sequences. Taking into account recent evolutionary cell biological discoveries, our data are most consistent with a scenario whereby the asgardarchaeal host cell was evolving cytoskeletal and membrane-protein machinery that was later incorporated into eukaryotic endomembrane systems following the acquisition of mitochondria and the evolution of sex.

evolutionary biology↗

bioRxiv2024

The metabolic costs of meiotic drive

Selfish genetic elements, such as meiotic drive genes, disrupt Mendels law of equal segregation by biasing their own transmission, often at a detriment to the rest of the genome. The Malaysian stalk-eyed fly (Teleopsis dalmanni) sex-ratio (SR) meiotic drive system is located within a series of large inversions on the X chromosome subject to low recombination and is associated with deleterious effects on fitness. Here we examine the metabolic effects of meiotic drive across male and female stalk-eyed flies. High-resolution O2k respirometry coupled with whole-organism respirometry were used to obtain mitochondrial function and metabolic rates. Complimentary assays on food consumption established downstream effects of metabolism on nutrient acquisition. The experiments demonstrate that individuals with SR meiotic drive elements have impaired mitochondrial function and reduced capacity for ATP synthesis, as shown by a lower respiratory control ratio and weaker contribution of Complex I to respiration. Drive individuals also exhibited an increased basal metabolic rate and consumed a greater amount of food than wild-type individuals. These findings show that the drive genotype imposes metabolic costs in both male and female hosts. The disruption in mitochondrial function likely leads to compensation via an increase in both basal metabolic rate and nutrient acquisition. A potential cause lies in the accumulation of deleterious mutations in the inversions on the X chromosome that house the meiotic drive, which are subject to weak natural selection. In females, the drive chromosome has a dominant effect, with a single copy causing substantial metabolic compromise. There was little evidence of male-specific metabolic costs, nor evidence of an accumulation of sexually antagonistic effects of drive chromosomes on female metabolism. These results suggest that direct metabolic costs from meiotic drive on spermatogenesis and from sexually antagonistic selection are relatively weak. This research provides new insight into the interplay between meiotic drive and metabolism, drawing attention to the broader physiological repercussions selfish genetic elements may have on their hosts.

evolutionary biology↗

bioRxiv2022

The establishment of locally adaptive inversions in structured populations

Inversions have been proposed to facilitate local adaptation, by linking together locally coadapted alleles at different loci. Classic prior work addressing this question theoretically has considered the spread of inversions in "continent-island" models in which there is a unidirectional flow of maladapted migrants into the island population. In this setting, inversions are most likely to establish when selection is weak, because stronger local selection more effectively purges maladaptive alleles, thus lessening the advantage of inversions. Here, we show this finding only holds under limited conditions. We study the establishment of inversions in a "two-deme" model, which explicitly considers the dynamics of allele frequencies in both populations linked by bidirectional migration. For symmetric selection and migration, we find that stronger local selection increases the flow of maladaptive alleles and favours inversions, the opposite of the pattern seen in the asymmetric continent-island model. Furthermore, we show that the strength and symmetry of selection also change the likelihood that an inversion captures an adaptive haplotype in the first place. Considering the combined process of invasion and capture shows that inversions are most likely to be found when locally adaptive loci experience strong selection. In addition, inversions that establish in one deme also protect adaptive allele combinations in the other, leading to differentiation between demes. Stronger selection in either deme once again makes differentiation between populations more likely. In contrast, differentiation is less likely when migration rates are high because adaptive haplotypes become less common. Overall, this analysis of evolutionary dynamics across a structured population shows that established inversions are most likely to have captured strongly selected local adaptation alleles.

evolutionary biology↗

bioRxiv2022

Meiotic drive does not impede success in sperm competition in the stalk-eyed fly, Teleopsis dalmanni

In male X-linked meiotic drive systems, the driver causes degeneration of Y-bearing sperm, leading to female-biased offspring sex ratios. This potentially leads to a two-fold transmission advantage to drive chromosomes. However, drive-bearing sperm often do poorly in sperm competition, limiting their ability to spread. We use the stalk-eyed fly, Teleopsis dalmanni, to investigate the success of the X-linked Sex Ratio (SR) meiotic drive system. In this species, polyandrous matings, where a female mates with multiple males, are common. Recent findings demonstrate SR males transfer the same numbers of viable sperm as wildtype (ST) males during mating, implying that they do not necessarily have reduced fertility under sperm competition. Reciprocal mating trials were performed to measure the success of SR and ST sperm in double mated females, with either a SR or ST male mated first followed by a male of the alternative genotype. There was no significant difference in the number of offspring sired by SR and ST males. This equivalence held regardless of whether the SR male mated first or second. We show these results are consistent with previous studies that suggested SR male sperm do poorly in sperm competition. Future experiments will determine whether the competitive ability of SR males is maintained under higher stress conditions likely to be experienced in nature, in which females mate repeatedly with multiple males. The results from the current study helps to explain the high meiotic drive frequency of around 20% in wild populations in this species. Impact SummaryMeiotic drive genes are selfish genetic elements that distort Mendelian patterns of inheritance to bias transmission in their favour. We use the stalk-eyed fly, Teleopsis dalmanni, to investigate the fitness effects associated with a meiotic drive gene called Sex Ratio (SR), which is linked to the X chromosome. In males, SR destroys Y-bearing sperm, meaning only X-bearing sperm are viable, and females who mate with drive males sire all-female broods. This confers a two-fold transmission advantage to the SR gene, as it is transmitted to all offspring. We recently discovered that drive males have evolved compensatory mechanisms to cope with the sperm destruction caused by meiotic drive. They have greatly enlarged testes, allowing them to produce more sperm. When drive males mate with females, they deliver as many sperm and sire as many offspring as wildtype males. Building on this finding, we measured how drive male sperm performs against sperm from a non-carrier male in sperm competition - where the sperm from different males compete to fertilise an egg. Double mating trials were performed, where a single female was mated once to a drive and once to a non-carrier male. By genotyping offspring, we show that the number of offspring sired by the drive male was not different from the number sired by the non-carrier competitor. These findings contrast with those in other species. Typically, drive males do poorly in sperm competition and their spread is severely restricted by sperm competition. In stalk-eyed flies, female multiple mating with many males is the norm, but this does not appear to inhibit the fertility of drive males. The success of drive under sperm competition helps to explain the high frequency of drive around 20% in natural populations of T. dalmanni.

evolutionary biology↗

bioRxiv2022

Meiotic drive adaptive testes enlargement during early development in the stalk-eyed fly.

The sex-ratio SR X-linked meiotic drive system in stalk-eyed flies destroys all Y-bearing sperm. Unlike other SR systems, drive males do not suffer fertility loss. They have greatly enlarged testes, which compensate for gamete killing. We predicted that enlarged testes arise from extended development with resources re-allocated from the accessory glands, as these tend to be smaller in drive males. To test this, we tracked the growth of the testes and accessory glands of wildtype and drive males over 5-6 weeks post-eclosion before males attained sexual maturity. Neither of the original predictions are supported by this data. Instead, we found that the drive-male testes were enlarged at eclosion, reflecting a greater allocation of resources to the testes during pupation. In addition, there was no evidence that the greater allocation of resources to the testes during adult development retarded accessory gland growth. There was evidence of a general trade-off with eyespan, as males with larger relative eyespan had larger accessory glands but smaller testes. These findings support the idea that enlarged testes in drive males arise as an adaptive allocation of resources to traits that enhance male reproductive success. One sentence summaryAdaptive testes enlargement in early development ensures maintenance of fertility in stalk-eyed flies that lose half of their sperm due to meiotic drive

evolutionary biology↗

bioRxiv2022

Repeat sequences limit the effectiveness of LGT and favoured the evolution of meiotic sex in early eukaryotes

The transition from prokaryotic lateral gene transfer to eukaryotic meiotic sex is poorly understood. Phylogenetic evidence suggests that it was tightly linked to eukaryogenesis, which involved an unprecedented rise in both genome size and the density of genetic repeats. Expansion of genome size raised the severity of Mullers ratchet, whilst limiting the effectiveness of lateral gene transfer (LGT) at purging deleterious mutations. In principle, an increase in recombination length combined with higher rates of LGT could solve this problem. Here we show using a computational model that this solution fails in the presence of genetic repeats prevalent in early eukaryotes. The model demonstrates that dispersed repeat sequences allow ectopic recombination, which leads to the loss of genetic information and curtails the capacity of LGT to prevent mutation accumulation. Increasing recombination length in the presence of repeat sequences exacerbates the problem. Mutational decay can only be resisted with homology along extended sequences of DNA. We conclude that the transition to homologous pairing along linear chromosomes was a key innovation in meiotic sex, which was instrumental in the expansion of eukaryotic genomes and morphological complexity. Relevance StatementThe origin of meiotic sex is a long-standing evolutionary enigma. This novel mechanism of reproduction replaced lateral gene transfer (LGT), the uptake and recombination of pieces of environmental DNA seen in bacteria and archaea. We link its origin to the expanded genome size and proliferation of genetic repeats found in early eukaryotes. Both factors led to high levels of mutation accumulation and gene loss under LGT which could not be retarded through increases in the rate of LGT or the length of DNA recombined. Meiotic sex with homologous pairing of long chromosome sized pieces of DNA promoted purifying selection and supressed ectopic recombination. It permitted the evolution of the expanded genome needed for the evolution of complex eukaryotic life.

evolutionary biology↗

bioRxiv2022

The limits of metabolic heredity in protocells

The universal core of metabolism could have emerged from thermodynamically favoured prebiotic pathways at the origin of life. Starting with H2 and CO2, the synthesis of amino acids and mixed fatty acids, which self-assemble into protocells, is favoured under warm anoxic conditions. Here we address whether it is possible for protocells to evolve greater metabolic complexity, through positive feedbacks involving nucleotide catalysis. Using mathematical simulations to model metabolic heredity in protocells, based on branch points in proto-metabolic flux, we show that nucleotide catalysis can indeed promote protocell growth. This outcome only occurs when nucleotides directly catalyse CO2 fixation. Strong nucleotide catalysis of other pathways (e.g. fatty acids, amino acids) generally unbalances metabolism and slows down protocell growth, and when there is competition between catalytic functions cell growth collapses. Autocatalysis of nucleotide synthesis can promote growth but only if nucleotides also catalyse CO2 fixation; autocatalysis alone leads to the accumulation of nucleotides at the expense of CO2 fixation and protocell growth rate. Our findings offer a new framework for the emergence of greater metabolic complexity, in which nucleotides catalyse broad-spectrum processes such as CO2 fixation, hydrogenation and phosphorylation important to the emergence of genetic heredity at the origin of life.

evolutionary biology↗

bioRxiv2020

The need for high-quality oocyte mitochondria at extreme ploidy dictates germline development

Selection against deleterious mitochondrial mutations is facilitated by germline processes, lowering the risk of genetic diseases. How selection works is disputed: experimental data are conflicting and previous modelling work has not clarified the issues. Here we develop computational and evolutionary models that compare the outcome of selection at the level of individuals, cells and mitochondria. Using realistic de novo mutation rates and germline development parameters, the evolutionary model predicts the observed prevalence of mitochondrial mutations and diseases in human populations. We show the importance of organelle-level selection, seen in the selective pooling of mitochondria into the Balbiani body, in achieving high-quality mitochondria at extreme ploidy in mature oocytes. Alternative mechanisms debated in the literature, bottlenecks and follicular atresia, are unlikely to account for the clinical data, because neither process effectively eliminates mitochondrial mutations under realistic conditions. Our findings explain the major features of female germline architecture, notably the longstanding paradox of over-proliferation of primordial germ cells followed by massive loss. The near-universality of these processes across animal taxa makes sense in light of the need to maintain mitochondrial quality at extreme ploidy in mature oocytes, in the absence of sex and recombination.

evolutionary biology↗

bioRxiv2020

X-linked meiotic drive boosts population size and persistence

X-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Selection for these selfish sex chromosomes can lead to completely female populations, which cannot produce offspring and go extinct. However, at the population level, moderately female-biased sex ratios are optimal because relatively few males are required to fertilise all the females. We develop eco-evolutionary models for sex-linked meiotic drive alleles to investigate their full range of demographic effects. We find general conditions for the spread and fixation of X-drivers, accounting for transmission bias and other factors associated with the spread of X-drivers such as sperm competition and polyandry. Our results suggest driving X-alleles that do not reach fixation (or do not bias segregation excessively) will boost population sizes and persistence times by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. We suggest that researchers should look beyond extinction risk and consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.

evolutionary biology↗

bioRxiv2020

Genome expansion in early eukaryotes drove the transition from lateral gene transfer to meiotic sex

Prokaryotes generally reproduce clonally but can also acquire new genetic material via lateral gene transfer (LGT). Like sex, LGT can prevent the accumulation of deleterious mutations predicted by Mullers ratchet for asexual populations. This similarity between sex and LGT raises the question why did eukaryotes abandon LGT in favor of sexual reproduction? Understanding the limitations of LGT provides insight into this evolutionary transition. We model the evolution of a haploid population undergoing LGT at a rate{lambda} and subjected to a mutation rate . We take into account recombination length, L, and genome size, g, neglected by previous theoretical models. We confirm that LGT counters Mullers ratchet by reducing the rate of fixation of deleterious mutations in small genomes. We then demonstrate that this beneficial effect declines rapidly with genome size. Populations with larger genomes are subjected to a faster rate of fixation of deleterious mutations and become more vulnerable to stochastic frequency fluctuations. Mullers ratchet therefore generates a strong constraint on genome size. Importantly, we show that the degeneration of larger genomes can be resisted by increases in the recombination length, the average number of contiguous genes drawn from the environment for LGT. Large increases in genome size, as in early eukaryotes, are only possible as L reaches the same order of magnitude as g. This requirement for recombination across the whole genome can explain the strong selective pressure towards the evolution of sexual cell fusion and reciprocal recombination during early eukaryotic evolution - the origin of meiotic sex.

evolutionary biology↗

bioRxiv2019

Does meiotic drive alter male mate preference?

Male mate preferences have been demonstrated across a range of species, including the Malaysian stalk-eyed fly, Teleopsis dalmanni. This species is subject to SR, an X-linked male meiotic driver, that causes the dysfunction of Y-sperm and the production all female broods. SR is associated with a low frequency inversion spanning most of the X chromosome that causes reduced organismal fitness. While there has been work considering female avoidance of meiotic drive males, the mating decisions of drive-bearing males have not been considered previously. As drive males are of lower genetic quality they may be less able to bear the cost of choice or may experience weaker selection for its maintenance if they are avoided by females. We investigated preference of drive males using binary choice trials. We confirmed that males prefer to mate with large females (indicative of greater fecundity) but found no evidence that the strength of male mate preference differs between drive and standard males. This suggests that the cost of choice does not restrict male reference among drive males. In a further experiment, we found that large eyespan males showed strong preference whereas small eyespan males showed no preference. This is likely to weaken mate preference in drive males, as on average they have reduced eyespan compared to standard males. In this respect, drive males are subject to and exert weak sexual selection.\n\nLay summaryWe studied male mate preference in stalk-eyed flies. This species suffers from meiotic drive, a selfish genetic element that causes a reduction in sperm production and organismal fitness. We predicted that males with meiotic drive would show weak mate preference. Males preferred to mate with large females, but there was no difference in the strength of preference between drive and non-drive males. Males with larger eyespan showed stronger mate preference. Meiotic drive males usually have reduced eyespan so on average they exert weaker sexual selection on females, but this is mediated by eyespan, not genotype per se.

evolutionary biology↗

bioRxiv2019

Meiotic drive reduces egg-to-adult viability in stalk-eyed flies

SR meiotic drive is a selfish genetic element located on the X chromosome in a number of species that causes dysfunction of Y-bearing sperm. SR is transmitted to up to 100% of offspring, causing extreme sex ratio bias. SR in several species is found in a stable polymorphism at a moderate frequency, suggesting there must be strong frequency-dependent selection resisting its spread. We investigate the effect of SR on female and male egg-to-adult viability in the Malaysian stalk-eyed fly, Teleopsis dalmanni. SR meiotic drive in this species is old, and appears to be broadly stable at a moderate (~20%) frequency. We use large-scale controlled crosses to estimate the strength of selection acting against SR in female and male carriers. We find that SR reduces the egg-to-adult viability of both sexes. In females, homozygous females experience greater reduction in viability (sf = 0.242) and the deleterious effects of SR are additive ([h] = 0.511). The male deficit in viability (sm = 0.214) is not different from that in homozygous females. The evidence does not support the expectation that deleterious side-effects of SR are recessive or sex-limited. We discuss how these reductions in egg-to-adult survival, as well as other forms of selection acting on SR, act to maintain SR polymorphism in this species.

evolutionary biology↗

bioRxiv2019

Adaptive maintenance of fertility in the face of meiotic drive

Selfish genetic elements that gain a transmission advantage through the destruction of sperm have grave implications for drive male fertility. In the X-linked SR meiotic drive system of a stalk-eyed fly, we found that drive males have greatly enlarged testes and maintain high fertility despite the destruction of half their sperm, even when challenged with fertilising large numbers of females. Conversely, we observed reduced allocation of resources to the accessory glands that probably explains the lower mating frequency of SR males. Body size and eyespan were also reduced, which are likely to impair viability and pre-copulatory success. We discuss the potential evolutionary causes of these differences between drive and standard males.

evolutionary biology↗

bioRxiv2019

Limits to environmental masking of genetic quality in sexual signals

There is considerable debate over the value of male sexual ornaments as signals of genetic quality. Studies alternately report that environmental variation enhances or diminishes the genetic signal, or leads to crossover where genotypes perform well in one environment but poorly in another. A unified understanding is lacking. We conduct the first experimental test examining the dual effects of distinct low and high genetic quality (inbred versus crossed parental lines) and low, through high, to extreme environmental stress (larval diets) on a condition-dependent male ornament. We find that differences in genetic quality signalled by the ornament (male eyespan in Diasemopsis meigenii stalk-eyed flies) become visible and are amplified under high stress but are overwhelmed in extreme stress environments. Variance among distinct genetic lines increases with environmental stress in both genetic quality classes, but at a slower rate in high quality outcrossed flies. Individual genetic lines generally maintain their ranks across environments, except among high quality lines under low stress conditions, where low genetic variance precludes differentiation between ranks. Our results provide a conceptual advance, demonstrating a unified pattern for how genetic and environmental quality interact. They show when environmental conditions lead to the amplification of differences in signals of genetic quality and thereby enhance the potential indirect genetic benefits gained by female mate choice.

evolutionary biology↗

bioRxiv2019

Evolution of the mating type locus with suppressed recombination

The two partners required for sexual reproduction are rarely the same. This pattern extends to species which lack sexual dimorphism yet possess self-incompatible gametes determined at mating-type regions of suppressed recombination, likely precursors of sex chromosomes. Here we investigate the role of cellular signaling in the evolution of mating-types. We develop a model of ligand-receptor dynamics within cells, and identify factors that determine the capacity of cells to send and receive signals. The model specifies conditions favoring the evolution of gametes producing ligand and receptor asymmetrically and shows how these are affected by recombination. When the recombination rate can evolve, the conditions favoring asymmetric signaling also favor tight linkage of ligand and receptor loci in distinct linkage groups. These results suggest that selection for asymmetric signaling between gametes was the first step in the evolution of non-recombinant mating-type loci, paving the road for the evolution of anisogamy and sexes.

evolutionary biology↗