Does genome size affect fitness in seed beetles?

Many of us think that the C-Value Paradox isn't really a paradox any more. We think that the variations in genome size among different species can be explained because expansion and contraction of genome size is mostly neutral with respect to evolution and thus the differing sizes of genomes in different species is explained by random genetic drift. Only a small percentage of most eukaryotic genomes is actually functional and the rest is junk. In the case of the human genome, about 90% is junk DNA.

Some scientists aren't happy with this explanation of the C-Value Paradox so they have come up with other explanations to account for the differences in genome sizes. A recent paper by Arnqvist et al. (2015) suggests that genome size affects reproductive fitness in seed beetles.

The introduction to their paper is a nice summary of the controversy ...

The general lack of correspondence between nuclear genome size (hence, GS) and organismal complexity is a classic problem in evolutionary biology [1,2]. Current hypotheses for the evolution of GS all rely on balancing forces which act to expand or to reduce GS. They can be broadly categorized into three non-mutually exclusive classes. First, the ‘junk DNA’ hypothesis recognizes that the selfish intragenomic propagation of transposons and other mobile genetic elements leads to the accumulation of mutations throughout the genome, yielding a one-way ticket to genomic obesity [3]. Such slightly deleterious mutations are then purged by very weak negative natural selection at the individual level [4–6], and the efficacy by which selection can rid the genome of mutationally hazardous DNA increases with increasing effective population size [7]. Second, the ‘selection hypothesis’ suggests that genomic reconfigurations associated with variation in GS has consequences for organismal fitness and that GS may, to a large extent, represent a dynamic balance between positive and negative selection on GS [8]. This could come about in many ways. For example, this hypothesis integrates the adaptive significance of gene duplication [9,10] and recent revaluations of the concept of ‘junk DNA’, suggesting that at least part of what was traditionally considered non-functional DNA may in fact have important effects on phenotypes [2,11–14]. Thirdly, a few other hypotheses do not involve natural selection on GS. For example, the ‘mutational equilibrium hypothesis’ suggests that GS represents a dynamic balance between DNA gain through large insertions and loss through small deletions, the rates of which are assumed to scale with GS [15]. Similarly, non-random assortative segregation by chromosome size during meiosis may, under some conditions, affect the evolution of GS [16].

It's hard to get an experimental handle on adaptive explanations because there are very few species where variation in genome size within a species is significant enough to test for fitness differences.

Theme
Genomes
& Junk DNAThere are 1350 known species of seed beetles¹. These insects lay their eggs in the seed of a legumous plant and the entire development of the insect (egg-larvae-pupa-adult) takes place within the seed. The authors looked at genome sizes in 12 different species of seed beetles and found that the size of the genome ranged from 704 Mb to 1486 Mb. (The human genome is 3,200 Mb.) It's unlikely that this two-fold difference reflects a difference in complexity since the two-fold variation occurs even within a genus (Callosobruchus). There was no correlation between genome size and population size, body size, or egg size.

Within the species Callosobruchus maculatus (cowpea seed beetle) there was a 4-5% difference in genome size among different populations that have been bred in the laboratory for various times over the past 40 years. This suggested a way to examine the effect of genome size in fitness by mating males and females with different sizes of genomes and measuring the number of offspring. Genome size within the species did not correlate with body size, development time, or growth rate but it did correlate with male and female reproductive success.

I've reproduced the key figure from the paper although I modified it somewhat to extend the x-axes to zero.

Their results show that both males and females with larger genomes are more successful at reproducing. There's a lot of scatter in the figure but the authors assure us that the correlation is significant.

Notice that the data for males (open circles) extrapolates back to zero fertilization success at a genome size of about 970 Mb. This seems a little strange since there are quite a few species of seed beetle that have genomes smaller than this. Presumably this will be investigated in future studies.

In addition to presenting positive evidence of selection for genome size, the authors discuss what they think is the lack of evidence for junk DNA. They note that there is no correlation between genome size and population size in the seed beetles. If the junk DNA advocates are correct then there should be a correlation, Arnqvist et al. according to

Here's the conclusion ...

In conclusion, we show that GS varies markedly both between and within seed beetle species and that GS shows rapid and bidirectional evolution. The pattern of evolution of GS is not consistent with a major role for genetic drift in shaping GS and GS did not show correlated evolution with estimates of species-specific relative population size. Within species, GS showed correlated evolution with both male and female reproductive fitness. Collectively, thus, our findings provide novel support for the hypothesis that GS variation results from natural selection in this clade.

What could cause a correlation between genome size and reproductive fitness? The authors suggest several reasons based on speculations by others about the possible function of excess DNA.

The observed positive link between GS and reproductive fitness could arise for several reasons, which are not mutually exclusive. For example, differences in the amount of non-coding DNA may reflect differences in the ability to regulate and fine-tune gene expression, such that larger genomes may be better able to produce phenotypes in high condition under a wider range of environments [2]. Further, differences in the amount of coding DNA may reflect adaptive gene duplication [9], allowing genotypes with larger genomes to be better buffered against deleterious mutations or otherwise be able to produce more adaptive phenotypes [10,54]. Yet another possibility is that variation in telomere length is positively related to reproductive fitness [55]. Alternatively, populations undergoing frequent laboratory bottlenecks may both be purged of deleterious alleles (due to inbreeding) and show larger GS (due to an increased importance of drift). We note, however, that laboratory populations of C. maculatus harbour genetic loads similar in magnitude to both wild populations and other seed beetle species [56,57] and the fact that we found no relationship between years-in-the-laboratory and GS offers no support for this scenario. Disentangling the above possibilities is currently not possible, as the relative contribution of coding and non-coding DNA to the GS variation seen in C. maculatus is unknown. Irrespective of the precise molecular causes of the documented association between genotype size and reproductive fitness, however, our results imply that natural selection acts on GS variation in our model system.

The Onion Test
by Ryan Gregory
I don't find the evidence convincing. Furthermore, even if there were a genuine correlation between genome size and reproductive fitness in this species of seed beetle, I don't think you can reasonably extrapolate this to onions.

None of the explanations make much sense and one of them (telomere length) is silly. I recognize that you don't need an explanation if the data is true—"unknown" is an acceptable answer—but we know enough about genomes and molecular biology to say that a cause and effect relationship is unlikely.

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1. Recall that God has a inordinate fondness for beetles [J.B.S. Haldane].

Arnqvist, G., Sayadi, A., Immonen, E., Hotzy, C., Rankin, D., Tuda, M., Hjelmen, C.E., and Johnston, J.S. (2015 Genome size correlates with reproductive fitness in seed beetles. Proc. Roy. Soc. (UK) B published online Sept. 9, 2015 [doi: 10.1098/rspb.2015.1421]