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Reproductive compensation and embryo screening drive the evolution of polyembryony

01 Sep 2021-bioRxiv (Cold Spring Harbor Laboratory)-

AbstractSimple polyembryony -- where one gametophyte produces multiple embryos with different sires but the same maternal haplotype -- is common in conifers, ferns, horsetails and other vascular plants. By providing a backup for inviable embryos, polyembryony may evolve as a mechanism of reproductive compensation. Alternatively, polyembryony may provide an opportunity for embryo screening and the preferential exclusion of low fitness embryos from the seed, perhaps acting as a mechanism of Self-Incompatibility (SI). To date, the evolution of polyembryony has not been modeled, and these verbal hypotheses have not been evaluated. We develop an infinite-site, forward population genetics model to test how these factors can favor the evolution of polyembryony, and how these underlying benefits of polyembryony shape the genetic load under a range of biological parameters. We find that reproductive compensation strongly favors the evolution of polyembryony, and embryo screening less strongly favors polyembryony. When embryo screening favors the evolution of polyembryony it increases embryo competitiveness, but does not act as an SI mechanism, as it does not trade low-fitness selfed offspring for high fitness outcrossed offspring. Remarkably we find nearly identical results in cases in which mutations impact either embryo or post-embryonic fitness (no pleiotropy), and in cases in which mutations have identical fitness effects embryo or post-embryonic fitness (extreme pleiotropy). In sum, the consequences of polyembryony depends on its function -- decreasing the mean embryonic fitness when acting as a mechanism of embryo compensation and increasing mean embryonic fitness when acting as a mechanism of screening.

Topics: Polyembryony (65%), Genetic load (53%)

Summary (3 min read)

Overview

  • To better understand how and when these factors favor the evolution of polyembryony, the authors vary the distribution of dominance and fitness effects and the probability of selfing.
  • When polyembryony does evolve, the authors ask how its evolution shapes the genetic load and its architecture.
  • The life cycle begins with N = 1000 diploid seeds, each of which has one or two embryos, depending on whether mothers are mono-or polyembryonic.
  • Following embryo selection, surviving seed parents for the next generation are chosen with replacement with a probability reflecting their post-embryonic fitness.

Parameters and model details

  • Genome structure and mutation rate: Every generation, each haploid genome expects a Poisson distributed number (mean U ) of de novo deleterious mutations to arise, each at any one of an infinite number of unlinked sites (i.e. an infinite sites model).
  • The authors investigate cases with U = 0.5 mutations per haploid chromosome per generation.
  • The authors focus on the case in which half of de novo deleterious mutations impact embryonic fitness and the other half impact post-embryonic fitness.
  • So the authors do not investigate this pleiotropic model here.
  • Both embryos of polyembryonic mothers are fertilized independently, and pollen parents of non-selfed seed are sampled with from the population with replacement in proportion to each genotypes post-embryonic fitness.

The distribution of fitness and dominance effects of new mutations:

  • To investigate the impact of mutational architecture on the evolution of polyembryony, the authors compare models with a different value of fitness (s), and dominance (h) effects of new mutations.
  • Thus, mutation effects span the range from quite deleterious to lethal, but will not reach fixation by random genetic drift.
  • In all simulations, the authors assumed that the distribution of fitness and dominance effects did not differ for mutations impacting the embryo and adult.
  • With a probability equal to the p self (which the authors systematically varied from zero to one in increments of 0.2) the seed parent was also chosen to be the pollen parent, also known as Selfing.
  • The authors note that this random mating does not preclude selfing.

Evolution

  • For all parameter combinations, the authors forward simulated ten replicates process for 2000 generations, ensuring that populations achieved mutationselection-drift balance by visually examining the variability in the number of deleterious mutations over time and among replicates .
  • For most parameter values, equilibrium was reached within this time frame .
  • For recessive mutations in predominantly outcrossing populations (with selfing rates of 0, 0.2, or 0.4) this was not enough time to reach equilibrium.
  • For these slowly equilibrating cases, the authors increased the burn-in period until 3000 generations, at which point equilibrium was largely achieved.
  • Finally, with complete selfing and a non-recessive load with s = 0.1, the number of deleterious mutations seems somewhat unstable .

Invasion of polyembryony:

  • For each burn in replicate, the authors ran many introductions of a dominant acting polyembryony allele, introduced at a frequency of 1/2N , and kept track of the fate of this allele (loss or fixation) for each introduction.
  • Due to computational considerations, the authors varied the number of introductions from 500 to 1000 for each model of polyembryony for each burn-in replicate.
  • That is, when polyembryony was strongly favored, a given simulation took longer to complete (because fixation from 1/2N takes more time than loss from 1/2N ).
  • The R (R Core Team 2020) code for these forward simulations is available on github https:.
  • In simple polyembryony with two embryos, the seed has three possible combinations of viable and inviable embryos.

Models of polyembryony

  • The authors aim to dissect the contribution of reproductive compensation and embryo competition to the evolution of polyembryony.
  • Thus, this model includes both potential benefits of polyembryony.
  • Each ovule in the seed of a polyembryonic genotype survives independently with a probability determined by its embryonic fitness.
  • As such, polyembryony provides the benefit of increasing the probability that a seed survives, but does not provide the added benefit of embryo competition.

Burn-in simulations

  • The authors discuss the results from their burn-in simulations, as they set the scene for the evolution of polyembryony.
  • Genomes saved at the end of the burn-in are available for download here.
  • Intriguingly, with an intermediate selfing rate of 0.4, the population appears to reach an equilibrium, relatively modest number of recessive mutations, until this rapidly and dramatically increases, presumably reflecting a transition from effective purging to interference among deleterious mutations (Lande et al.
  • The authors observe a strong positive correlation between embryo and post-embryo fitness for recessive gene action and intermediate selfing rates, but no relationship otherwise (Fig. 3D , and Fig. S2D ).

Invasion of polyembryony

  • The authors compare the fixation probability of a new mutant that confers polyembryony, across all models described above.
  • The dashed pink line displays the expectation under neutrality.
  • In cases with additive gene action, the fixation probability of a polyembryony allele decreases with the selfing rate, again reflecting the lack of within-seed variance in fitness.
  • The benefit of embryo competition also favors the evolution of polyembryony.
  • Fixation probabilities are approximately five-to ten-fold lower for this model than for the reproductive compensation model.

Evolutionary consequences of polyembryony

  • The authors compare how different models of the evolution of polyembryony shape key features of a population, including the proportion of surviving seeds, the realized selfing rate and the architecture of genetic load.
  • The benefit of compensation (in both the compensation and all benefits model) resulted in a strong increase in seed survival.
  • Higher fitness embryos, the benefit of competition alone subtly increased seed survival for all models of dominance investigated so long as the selfing rate was not too large (Fig. 5 ).
  • Figure 6 shows that the allele frequency spectrum is comparable in the no benefit and competition model, arguing against the idea that competition favored selfsacrifice in the form of an excess of rare recessive lethals.
  • By contrast, there is a slight increase in the count of deleterious recessive mutations across all frequency classes in the compensation and all benefits models, reflecting the relaxation of embryo selection in these cases.

Discussion

  • The authors present four models to test the plausibility of the compensation and competition theories for the evolution of polyembryony.
  • By contrast, the benefit of embryo competition more weakly favored the evolution of polyembryony, resulting in between a zero-fold increase with high selfing rates, and a twenty-fold increase, with intermediate to low selfing rates and a recessive load, relative to neutral expectations.
  • As such, embryo competition does not offer a more refined view into postembryo fitness than is automatically accounted for by "hard selection" on seed viability imposed in their model.
  • That is, the authors must consider biological processes outside of their model as they interpret their model results.
  • Competition, compensation and conflict in a pine nutshell: Gymnosperm seed with a maternal haploid megagametophyte, multiple geneti-cally distinct embryos, genetically identical embryos, and strong inbreeding depression is a stage of evolutionary drama that deserves more attention, and the authors hope that the provided model will be used to broaden the investigations on the evolutionary dynamics outside the angiosperm sphere.

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Reproductive compensation and embryo
competition drive the evolution of polyembryony
November 17, 2020
Institutional affiliations
Yaniv Brandvain: Department of Plant and Microbial Biology, University
of Minnesota, St. Paul, Minnesota 55108
Alexander Harkness: Department of Ecology, Evolution, and Behavior, Uni-
versity of Minnesota, St. Paul, Minnesota 55108
Tanja Pyh¨aj¨arvi: Department of Ecology and Genetics, University of Oulu,
FI-90014 Oulu, Finland.
Corresponding author contact details
Corresponding author: Yaniv Brandvain. 1500 Gortner Ave. St. Paul, MN,
USA 55108. ybrandva@umn.edu
Keywords
Self-Incompatibility
Polyembryony
Sibling Rivalry
1
.CC-BY-NC-ND 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted November 17, 2020. ; https://doi.org/10.1101/2020.11.17.387340doi: bioRxiv preprint

Abstract1
Simple polyembryony where a single gametophyte produces2
multiple embryos with different sires but the same maternal hap-3
lotype is common in conifers, ferns, horsetails and other vas-4
cular plants. Polyembryony could be favored as a mechanism of5
reproductive compensation, providing a backup for inviable em-6
bryos, or as a mechanism of embryo competition and eliminating7
plants with low tness, perhaps acting as a mechanism of Self-8
Incompatibility (SI). However as the evolution of polyembryony9
from monoembryony has not been modeled these long standing10
verbal models have not been evaluated. We develop an infinite-11
site, forward population genetics model to test how these factors12
can favor the evolution of polyembryony, and how these under-13
lying benefits of polyembryony shape the genetic load under a14
range of selfing rates, dominance, and selection coefficients. We15
find that the benefit of reproductive compensation strongly fa-16
vors the evolution of polyembryony, while the benefits of embryo17
competition are much weaker. Importantly, when embryo com-18
petition favors the evolution of polyembryony it increases embryo19
competitiveness, but does not act as an SI mechanism, as it does20
not effectively trade low-fitness selfed offspring for high fitness21
outcrossed offspring. We find that the impact of polyembryony22
on the genetic load depends on its function increasing the em-23
bryo load when acting as a mechanism of embryo compensation24
and decreasing the embryo load when acting as a mechanism of25
competition.26
.CC-BY-NC-ND 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted November 17, 2020. ; https://doi.org/10.1101/2020.11.17.387340doi: bioRxiv preprint

Nature is, above all, profligate. Don’t believe them when they27
tell you how economical and thrifty nature is.28
Annie Dillard 1974.29
Not only do most parents produce more offspring than will survive, but30
most organisms that provide parental care make more offspring than they31
will likely be able to nurture to independence. Frequent siblicide in the great32
egret, Casmerodius albus, provides a dramatic example of this siblings kill33
one another, presumably over the ability to monopolize small food items34
(Mock 1984); Why then do egret mothers continue laying eggs that will35
develop into offspring that will kill one another? Could such overproduction36
allow parents to screen for offspring quality (Forbes and Mock 1998), or37
does the “diverse portfolio” of offspring born over the breeding season allow38
parents to hedge their bets (Forbes 2009)?39
Simple polyembryony provides an even more extreme, but perhaps less40
dramatic, example of this problem. With simple polyembryony, a single ma-41
ternal gametophyte is fertilized by multiple sperm cells to produce multiple42
embryos with genetically identical maternally derived genomes but distinct43
paternal genomes (Buchholz 1922; Schnarf 1937, cited in Dogra 1967). Here44
we present an infinite sites forward-in-time population genomic simulation45
to test the competition (akin to egret mothers screening for offspring qual-46
ity) and compensation (akin to egret mothers hedging their bets) theories47
for the evolution of polyembryony, and to investigate how polyembryony48
changes the genetic architecture of embryonic and postembryonic fitness.49
Simple polyembryony is ubiquitous in gymnosperms (Willson and Bur-50
ley 1983), and is found in many seedless vascular plants including ferns and51
horsetails (Buchholz 1922). The number of archegonia per seed typically52
.CC-BY-NC-ND 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted November 17, 2020. ; https://doi.org/10.1101/2020.11.17.387340doi: bioRxiv preprint

varies from two to four in the genus Pinus, but can reach up to 200 (as re-53
ported in Widdringtonia juniperoides Saxton 1934). In gymnosperms, from54
this base of numerous archegonia, typically only a single embryo survives in55
mature seed (Chamberlain 1966).56
Evolutionary theorists have investigated the evolutionary consequences57
of polyembryony specifically how polyembryony (or less mechanistically58
explicit forms of reproductive compensation) could shape the genetic load59
(Latta 1995; Sakai 2019; Porcher and Lande 2005; arkk¨ainen et al. 1996)60
and the exposure of inbreeding depression (K¨arkk¨ainen and Savolainen 1993;61
Hedrick et al. 1999). However, theories for the evolutionary origin of sim-62
ple polyembryony are less well developed. Here, we develop theory for the63
evolution of simple polyembryony. We do not consider cleavage polyembry-64
ony, in which a fertilized zygote can split into numerous genetically identical65
embryos (Agapito-Tenfen et al. 2012), or nucellar polyembryony, in which66
maternal tissue asexually develops into embryos (Lakshmanan and Ambe-67
gaokar 1984), sometimes competing with sexually derived embryos, as they68
are likely favored by distinct mechanisms (Ganeshaiah et al. 1991).69
We consider the two major advantages of simple polyembryony described70
by arkk¨ainen and Savolainen (1993): reproductive compensation im-71
proved seed set, and embryo competition the potentially improved post-72
embryonic fitness of surviving embryos compared to the projected fitness73
of unsuccessful embryos (Sorensen 1982; Porcher and Lande 2005). Repro-74
ductive compensation is an increase in seed set that occurs when embryo75
mortality is counteracted by an expanded supply of embryos. Polyembryony76
provides reproductive compensation if a lone embryo is less likely to develop77
into a successful seed than is a collection of sibling embryos. So, for exam-78
ple, if a proportion p of embryos are inviable, a second embryo increases the79
.CC-BY-NC-ND 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted November 17, 2020. ; https://doi.org/10.1101/2020.11.17.387340doi: bioRxiv preprint

probability that a seed contains a surviving embryo from 1 p to 1 p
2
80
(Lindgren 1975).81
Alternatively, if embryonic and post-embryonic fitness a positively cor-82
related, embryo competition (dubbed Developmental Selection by Buchholz83
(1922)), could favor the evolution of polyembryony. Such a correlation can84
arise either through pleiotropy across the life cycle, or if embryonic fitness85
determined by one set of loci predicted post-embryonic fitness produced by86
another set of loci. This later option seems particularly likely if inbred87
offspring are unfit across the life cycle, and as such, simple polyembryony88
is often interpreted as an inbreeding avoidance mechanism (e.g. Dogra89
1967; Sorensen 1982) analogous to the self-incompatibility systems (here-90
after SI) found in angiosperms. Koski (1971) and others contend that this91
gives way to evolution of the so-called “Embryo Lethal System” an ap-92
parently coordinated self destruction mechanism revealed upon inbreeding93
(Koski 1971; Sarvas 1962, e.g. page 162 onwards ) in pines as a mech-94
anism evolved to prevent selfing. Under this model, polyembryony does95
not prevent self-fertilization per se, but dampens self-fertilization’s delete-96
rious effects by allowing competition and something of a maternal choice97
among the selfed and outcrossed progeny before major maternal resource98
allocation (Willson and Burley 1983; Sorensen 1982). This potential form99
of postzygotic mate choice could circumvent the constraint imposed by the100
unenclosed gymnosperm seed, which precludes prezygotic mate choice (e.g.101
SI systems Dogra 1967; Sorensen 1982; Willson and Burley 1983).102
Critically, the embryo competition model assumes that possibility of ef-103
fective competition between embryos in a seed, a topic of much debate.104
Based on extensive experimental work on P. sylvestris, Sarvas (1962) stated105
that embryo competition and “struggle for life” is quite apparent under mi-106
.CC-BY-NC-ND 4.0 International licenseavailable under a
(which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made
The copyright holder for this preprintthis version posted November 17, 2020. ; https://doi.org/10.1101/2020.11.17.387340doi: bioRxiv preprint

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