Interacting cells driving the evolution of multicellular life cycles

Author summary Multicellular organisms are ubiquitous. But how did the first multicellular organisms arise? It is typically argued that this occurred due to benefits coming from interactions between cells. One example of such interactions is the division of labour. For instance, colonial cyanobacteria delegate photosynthesis and nitrogen fixation to different cells within the colony. In this way, the colony gains a growth advantage over unicellular cyanobacteria. However, not all cell interactions favour multicellular life. Cheater cells residing in a colony without any contribution will outgrow other cells. Then, the growing burden of cheaters may eventually destroy the colony. Here, we ask what kinds of interactions promote the evolution of multicellularity? We investigated all interactions captured by pairwise games and for each of them, we look for the evolutionarily optimal life cycle: How big should the colony grow and how should it split into offspring cells or colonies? We found that multicellularity can evolve with interactions far beyond cooperation or division of labour scenarios. More surprisingly, most of the life cycles found fall into either of two categories: A parent colony splits into two multicellular parts, or it splits into multiple independent cells

The possible modes of microbial reproduction are fundamentally restricted by distribution of mass between parent and offspring

SignificanceCells and simple cell colonies reproduce by fragmenting their bodies into pieces. Produced newborns need to grow before they can reproduce again. How big a cell or a cell colony should grow? How many offspring should be produced? Should they be of equal size or diverse? We show that the simple fact that the immediate mass of offspring cannot exceed the mass of parents restricts possible answers to these questions. For example, our theory states that, when mass is conserved in the course of fragmentation, the evolutionarily optimal reproduction mode is fragmentation into exactly two, typically equal, parts. Our theory also shows conditions which promote evolution of asymmetric division or fragmentation into multiple pieces

Eco-evolutionary dynamics of clonal multicellular life cycles

The evolution of multicellular life cycles is a central process in the course of the emer-gence of multicellularity. The simplest multicellular life cycle is comprised of the growth of the propagule into a colony and its fragmentation to give rise to new propagules. The majority of theo-retical models assume selection among life cycles to be driven by internal properties of multicellular groups, resulting in growth competition. At the same time, the influence of interactions between groups on the evolution of life cycles is rarely even considered. Here, we present a model of colo-nial life cycle evolution taking into account group interactions. Our work shows that the outcome of evolution could be coexistence between multiple life cycles or that the outcome may depend on the initial state of the population – scenarios impossible without group interactions. At the same time, we found that some results of these simpler models remain relevant: evolutionary stable strategies in our model are restricted to binary fragmentation – the same class of life cycles that contains all evolutionarily optimal life cycles in the model without interactions. Our results demonstrate that while models neglecting interactions can capture short- term dynamics, they fall short in predicting the population- scale picture of evolution

Why is cyclic dominance so rare?

Natural populations can contain multiple types of coexisting individuals. How does natural selection maintain such diversity within and across populations? A popular theoretical basis for the maintenance of diversity is cyclic dominance, illustrated by the rock-paper-scissor game. However, it appears difficult to find cyclic dominance in nature. Why is this the case? Focusing on continuously produced novel mutations, we theoretically addressed the rareness of cyclic dominance. We developed a model of an evolving population and studied the formation of cyclic dominance. Our results showed that the chance for cyclic dominance to emerge is lower when the newly introduced type is similar to existing types compared to the introduction of an unrelated type. This suggests that cyclic dominance is more likely to evolve through the assembly of unrelated types whereas it rarely evolves within a community of similar types

Evolution of reproductive strategies in incipient multicellularity

Multicellular organisms potentially show a large degree of diversity in reproductive strategies, producing offspring with varying sizes and compositions compared to their unicellular ancestors. In reality, only a few of these reproductive strategies are prevalent. To understand why this could be the case, we develop a stage-structured population model to probe the evolutionary growth advantages of reproductive strategies in incipient multicellular organisms. The performance of reproductive strategies is evaluated by the growth rates of the corresponding populations. We identify the optimal reproductive strategy, leading to the largest growth rate for a population. Considering the effects of organism size and cellular interaction, we found that distinct reproductive strategies could perform uniquely or equally well under different conditions. If a single reproductive strategy is optimal, it is binary splitting, dividing into two parts. Our results show that organism size and cellular interaction can play crucial roles in shaping reproductive strategies in nascent multicellularity. Our model sheds light on understanding the mechanism driving the evolution of reproductive strategies in incipient multicellularity. Beyond multicellularity, our results imply that a crucial factor in the evolution of unicellular species’ reproductive strategies is organism size

Evolution of irreversible somatic differentiation

A key innovation emerging in complex animals is irreversible somatic differentiation: daughters of a vegetative cell perform a vegetative function as well, thus, forming a somatic lineage that can no longer be directly involved in reproduction. Primitive species use a different strategy: vegetative and reproductive tasks are separated in time rather than in space. Starting from such a strategy, how is it possible to evolve life forms which use some of their cells exclusively for vegetative functions? Here, we developed an evolutionary model of development of a simple multicellular organism and found that three components are necessary for the evolution of irreversible somatic differentiation: (i) costly cell differentiation, (ii) vegetative cells that significantly improve the organism’s performance even if present in small numbers, and (iii) large enough organism size. Our findings demonstrate how an egalitarian development typical for loose cell colonies can evolve into germ-soma differentiation dominating metazoans.Competing Interest StatementThe authors have declared no competing interest

Limb reduction in squamate reptiles correlates with the reduction of the chondrocranium: A case study on serpentiform anguids

Abstract Background In vertebrates, the skull evolves from a complex network of dermal bones and cartilage?the latter forming the pharyngeal apparatus and the chondrocranium. Squamates are particularly important in this regard as they maintain at least part of the chondrocranium throughout their whole ontogeny until adulthood. Anguid lizards represent a unique group of squamates, which contains limbed and limbless forms and show conspicuous variation of the adult skull. Results Based on several emboadryonic stages of the limbless lizards Pseudopus apodus and Anguis fragilis, and by comparing with other squamates, we identified and interpreted major differences in chondrocranial anatomy. Among others, the most important differences are in the orbitotemporal region. P. apodus shows a strikingly similar development of this region to other squamates. Unexpectedly, however, A. fragilis differs considerably in the composition of the orbitotemporal region. In addition, A. fragilis retains a paedomorphic state of the nasal region. Conclusions Taxonomic comparisons indicate that even closely related species with reduced limbs show significant differences in chondrocranial anatomy. The Pearson correlation coefficient suggests strong correlation between chondrocranial reduction and limb reduction. We pose the hypothesis that limb reduction could be associated with the reduction in chondrocrania by means of genetic mechanisms

Whispering gallery modes in open quantum billiards

The poles of the S-matrix and the wave functions of open 2D quantum billiards with convex boundary of different shape are calculated by the method of complex scaling. Two leads are attached to the cavities. The conductance of the cavities is calculated at energies with one, two and three open channels in each lead. Bands of overlapping resonance states appear which are localized along the convex boundary of the cavities and contribute coherently to the conductance. These bands correspond to the whispering gallery modes appearing in the classical calculations.Comment: 9 pages, 3 figures in jpg and gif forma

S-matrix theory for transmission through billiards in tight-binding approach

In the tight-binding approximation we consider multi-channel transmission through a billiard coupled to leads. Following Dittes we derive the coupling matrix, the scattering matrix and the effective Hamiltonian, but take into account the energy restriction of the conductance band. The complex eigenvalues of the effective Hamiltonian define the poles of the scattering matrix. For some simple cases, we present exact values for the poles. We derive also the condition for the appearance of double poles.Comment: 29 pages, 9 figures, submitted to J. Phys. A: Math. and Ge

Hall-like effect induced by spin-orbit interaction

The effect of spin-orbit interaction on electron transport properties of a cross-junction structure is studied. It is shown that it results in spin polarization of left and right outgoing electron waves. Consequently, incoming electron wave of a proper polarization induces voltage drop perpendicularly to the direct current flow between source and drain of the considered four-terminal cross-structure. The resulting Hall-like resistance is estimated to be of the order of 10^-3 - 10^-2 h/e^2 for technologically available structures. The effect becomes more pronounced in the vicinity of resonances where Hall-like resistance changes its sign as function of the Fermi energy.Comment: 4 pages (RevTeX), 4 figures, will appear in Phys. Rev. Let