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

Abstract

Significance Cells 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

“…Colonies are born small, but due to cell divisions they increase in size and, eventually, fragment, so the number of colonies in the population increases. The life cycle maximizing the population growth rate has a selective advantage as it outgrows all competitors ( Roze and Michod, 2001 ; Libby et al, 2014 ; Pichugin et al, 2017 ; Pichugin et al, 2019 ; Staps et al, 2019 ; Gao et al, 2019 ; Pichugin and Traulsen, 2020 ; Gao et al, 2021 ; Pichugin, 2022 ; Pichugin and Traulsen, 2022 ). For groups made of identical cells, growth competition models of evolution predict that some life cycles cannot be the winners of this growth competition under any conditions.…”

The role of the unicellular bottleneck and organism size in mediating cooperation and conflict among cells at the onset of multicellularity

“…One of our key new results is the dominance of life cycles other than binary fragmentation. Previous models have found binary fragmentation to dominate whether considering discrete or continuous time (Pichugin and Traulsen, 2022), exponential or frequency-dependent growth (Pichugin et al 2017, Ress et al 2022), or even when considering bidirectional switching between two cell types (Gao et al 2019). Here, however, we find modes that produce multiple offspring to dominate under a wide range of conditions.…”

“…In nature, binary fragmentation is common. For example, Trichoplax adhaerens reproduces via binary fission and bacterial biofilms reproduce via the unicellular propagule strategy (Pichugin and Trauslen 2022;Ratcliff et al 2017). But other fragmentation modes are also found.…”

“…This fragmentation framework captures the diversity of life-cycles we see in nature. For example, Trichoplax adhaerens reproduces via binary fission and bacterial biofilms reproduce via the unicellular propagule mode (Pichugin and Traulsen 2022; Ratcliff et al 2017). Meanwhile, species in the genera Chlamydomonas and Gonium reproduce via multiple fission (Hanschen et al 2016; Pichugin and Traulsen 2022), as do Acoelomorpha worms, sea stars and sea cucumbers (Howe et al 2022, Mladenov 1996).…”

Eco-evolutionary dynamics of clonal multicellular life cycles

“…Colonies are born small but due to cell divisions they increase in size and, eventually, fragment, so the number of colonies in the population grows. The life cycle maximizing the population growth rate has a selective advantage, as it outgrows all competitors [Roze et al, 2001, Libby et al, 2014, Pichugin et al, 2017, 2019, Staps et al, 2019, Gao et al, 2019, Pichugin and Traulsen, 2020, Gao et al, 2021, Pichugin and Traulsen, 2022]. It was shown that for groups made of identical cells, some life cycles are forbidden: they cannot be the winner of growth competition under any conditions.…”