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Danube crested newt (Triturus dobrogicus)

In evolutionary biology, a balanced lethal system is a situation where recessive lethal alleles are present on two homologous chromosomes.[1] Each of the chromosomes in such a pair carries a different lethal allele, which is compensated for by the functioning allele on the other chromosome.[1] Since both these lethal alleles end up in the gametes in the same frequency as the functioning alleles, half of the offspring, the homozygotes, receive two copies of a lethal allele and therefore die during development.[1] In such systems, only the heterozygotes survive.[1]

Balanced lethal systems appear to pose a challenge to evolutionary theory, since a system so wasteful should be rapidly eliminated through natural selection and recombination.[2] Instead, it has become fixed in various species all over the tree of life.[1][2]

Mechanism

The exact mechanism behind balanced lethal systems remains unknown. Prior to the availability of efficient DNA sequencing methods, it was already known that the lethality in such a system was caused by homozygosity of a certain chromosome pair.[3][4]

One theory is that, in the case of the Triturus genus, the balanced lethal system is a remnant of an ancient sex-determination system.[1][2] One of the chromosomes of the pair that contains the system is longer than the other, which is also the case for the actual sex chromosomes.[2] In this theory, deleterious mutations accumulated on the non-recombining part of the Y-chromosome (Muller’s ratchet).[1][2][5] Then, two distinct Y-chromosomes, both with different lethal mutations, co-segregated in a population.[1] Since sex-determination in many cold-blooded vertebrates is potentially dependent on temperature, a shift away from chromosomal sex determination occurred.[1][2] This system favoured the sex reversal of females, which eventually led to the loss of the original X-chromosome.[1][2] A mutation on another chromosome later restored the even sex ratio, and gave rise to a new male-heterogametic system.[1][2] A major restriction for this theory is that it could only evolve in species where temperature-dependent sex-reversal is possible.[1] Since balanced lethal systems are found in many species where this is not the case, this theory does not provide a general explanation for how such a system evolved.[1]

Another theory is that balanced lethal systems are collapsed supergenes.[1] Supergenes are linked genes that are inherited as a single unit.[6] Genes can only be inherited together when recombination is suppressed, for example when selection favors certain allelic combinations.[6] The lack of recombination can lead to the accumulation of mutations in both supergene clusters[1][6] and this could generate a feedback loop:[1] when natural selection favours heterozygotes, few homozygotes reproduce.[1] This lack of reproduction leads to the accumulation of deleterious alleles. When lethal mutations become fixed on both supergene alleles, homozygotes are no longer viable, resulting in a balanced lethal system.[1]

Prevalence

A well known balanced lethal system is the one fixed in the genus Triturus (containing the crested and the marbled newts).[4] Each of the homologous chromosomes of pair 1 (1A and 1B) has a different recessive deleterious allele on a non-recombining section of the chromosome.[2] Therefore, only heterozygotes are viable since these deleterious alleles are compensated for by the functioning allele on the other homologue. As a result half of all offspring stop growing and die during early development.[2]

The offspring of Triturus carnifex for example, have either a viable heterozygous genotype (1A/1B) or one of the homozygous embryonic lethal genotypes: fat-tailed (1A/1A) or slim-tailed (1B/1B).[7]

See also

References

  1. ^ a b c d e f g h i j k l m n o p q r Wielstra B (July 2020). "Balanced lethal systems". Current Biology. 30 (13): R742–R743. doi:10.1016/j.cub.2020.05.011. hdl:1887/135621. PMID 32634409. S2CID 220366171.
  2. ^ a b c d e f g h i j Grossen C, Neuenschwander S, Perrin N (December 2012). "The balanced lethal system of crested newts: a ghost of sex chromosomes past?". The American Naturalist. 180 (6): E174-83. doi:10.1086/668076. PMID 23149410. S2CID 7724949.
  3. ^ Callan HG, Lloyd L (1960-11-24). "Lampbrush chromosomes of crested newts Triturus cristatus (Laurenti)". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 243 (702): 135–219. Bibcode:1960RSPTB.243..135C. doi:10.1098/rstb.1960.0007. S2CID 84478833.
  4. ^ a b Macgregor HC, Horner H (January 1980). "Heteromorphism for chromosome 1, a requirement for normal development in crested newts". Chromosoma. 76 (2): 111–122. doi:10.1007/BF00293412. S2CID 3050214.
  5. ^ Berdan EL, Blanckaert A, Butlin RK, Bank C (March 2021). Buerkle A (ed.). "Deleterious mutation accumulation and the long-term fate of chromosomal inversions". PLOS Genetics. 17 (3): e1009411. doi:10.1371/journal.pgen.1009411. PMC 7963061. PMID 33661924.
  6. ^ a b c Black D, Shuker DM (July 2019). "Quick Guide Supergenes" (PDF). Current Biology. 29 (13): R603–R622. doi:10.1016/j.cub.2019.05.024. PMID 31287973. S2CID 208789090.
  7. ^ Wallace H (July 1994). "The balanced lethal system of crested newts". Heredity. 73 (1): 41–46. doi:10.1038/hdy.1994.96. S2CID 39406562.

Further reading

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