The recent increase in genomic data is revealing a novel perspective of gene loss as a pervasive source of genetic variation in all life kingdoms.
Gene loss depends on gene dispensability, which in turn is affected by changes in mutational robustness and environmental conditions.
Patterns of gene loss are not stochastic but show biases that are associated with gene functions and genomic positions.
Although many gene losses are neutral and fixed by genetic drift, many examples support the idea that gene loss can be an adaptive evolutionary force that is especially effective when organisms are faced with abrupt environmental challenges.
The future mapping of all instances of gene loss in the tree of life will provide valuable information for many fields of biology, including evolutionary biology and translational medicine.
Population genomics might expose ongoing processes of gene loss in natural populations, revealing actual values of gene dispensability and identifying adaptive gene losses with potential interest in biomedicine.
The recent increase in genomic data is revealing an unexpected perspective of gene loss as a pervasive source of genetic variation that can cause adaptive phenotypic diversity. This novel perspective of gene loss is raising new fundamental questions. How relevant has gene loss been in the divergence of phyla? How do genes change from being essential to dispensable and finally to being lost? Is gene loss mostly neutral, or can it be an effective way of adaptation? These questions are addressed, and insights are discussed from genomic studies of gene loss in populations and their relevance in evolutionary biology and biomedicine.
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The authors thank the interesting and helpful comments of the three anonymous thoughtful referees. The authors apologize to the researchers whose work has not been directly cited owing to space restrictions. Support is acknowledged from past grant BFU2010-14875 from Ministerio de Economía y Competitividad (Spain) and SGR2014-290 from Generalitat de Catalunya. The authors also thank the team members of the Cañestro and Albalat laboratories for fruitful discussions on Oikopleura's passion for gene loss.
The authors declare no competing financial interests.
Supplementary information S1 (table)
Examples of gene losses associated to parasitic/endosymbiontic life styles (PDF 142 kb)
Supplementary information S2 (table)
Examples of gene losses in animals concomitant with the evolution of new biological features (PDF 158 kb)
Supplementary information S3 (box)
Supplementary information (PDF 118 kb)
An evolutionary phenomenon whereby a gene loses its function, accumulates mutations and becomes a pseudogene.
Clade that classically includes all animals (metazoan) except sponges and Placozoa, although recent analyses of ctenophores have challenged the monophyly of this group.
Genes that share sequence similarity because they have evolved from a common ancestral gene.
An animal clade that includes protostomes and deuterostomes. Members of this clade are characterized by a stage during their life cycle in which they have right–left symmetry (unlike the radial symmetry present in most cnidarians and sponges).
A superphylum that includes animals in which the first opening, the blastopore, becomes the anus. This superphylum includes Ambulacraria (hemichordates and echinoderms) and Chordates (cephalochordates, urochordates and vertebrates).
A superphylum that includes animals in which the first opening, the blastopore, becomes the mouth. This superphylum includes two groups: Ecdysozoa (for example, arthropods and nematodes) and Lophotocozoa (for example, molluscs, annelids and platyhelminthes).
- Propensity for gene loss
Proclivity of a gene to be lost during evolution of a clade, as estimated from the fraction of lineages in which a given gene has been lost and corrected by the time during which the gene was lost or preserved.
- 'Patchy' orthologues
Orthologues belonging to gene families that have suffered extensive gene loss during the evolution of a given clade, such that their presence is unevenly distributed and restricted to a few species in the clade.
A hypothetical subkingdom that includes all animals apart from poriferans and ctenophores based on the absence of homeobox (Hox)–ParaHox genes from the first sequenced species of the later groups.
A term coined in honour of Susumo Ohno that refers to paralogues that originated from genome duplication (in contrast to paralogues that originated from small-scale duplications).
Acquisition of additional genetic content due to whole-genome duplication.
- Reductive evolution
Refers to the loss of genetic material that is usually observed during the evolution of parasitic or symbiotic species.
The ability of a particular genotype (or phenotype) to survive and reproduce in a specific environment, which is usually expressed in relation to other possible genotypes.
- Developmental genetic toolkits
Sets of genes that are required for development and that are widely shared among species.
- Mutational robustness
Property of a biological system to maintain unaltered phenotypes in the face of mutations.
- Synthetic genetic array
(SGA). Methodology designed to map genetic interactions on a genome-wide scale that combines arrays of mutant strains with robotic manipulations for high-throughput double-mutant construction.
- Synthetic lethality
This occurs when a combination of mutations in two or more genes leads to death, but when no effects on the viability of the organism are apparent when the genes are mutated individually.
- Cryptic variation
Genetic diversity within a population that does not normally generate phenotypic diversity but that does occur on environmental or genetic perturbation.
- Flux balance analyses
(FBAs). Mathematical approaches for calculating the flow of metabolites through a metabolic network, which can be applied to reconstruct genome-scale metabolic networks and to predict the growth rate of an organism.
- Gene Ontology
(GO). A system for classification of genes in terms of their associated biological processes, cellular components and molecular functions in a species-independent manner.
- Conserved synteny
Conservation of similar blocks of genes between orthologous or paralogous chromosomal regions, which can be useful in detecting gene losses after speciation or large-scale genomic duplications, respectively.
- Reciprocal gene loss
Divergent resolution of gene duplicates, such that one species has lost one copy, whereas the second species has lost the other copy.
- Baker's rule
This rule states that self-compatible organisms are better colonizers after long-distance dispersal than self-incompatible ones.
- Genetic drift
Stochastic changes in allele frequencies in a population due to random sampling effects through successive generations, which is therefore highly affected by the population size.
- Gene loss rate
(GLR). The maximum likelihood estimate of the measure of gene loses that maximizes the probability of the phyletic pattern of presence and absence of a given gene considering estimated branch lengths of all possible ancestral phylogenetic trees for the species under study.
- Antagonistic pleiotropy
This occurs when a gene controls several traits, in which at least one of these traits is beneficial to the organism's fitness and at least one is detrimental to the organism's fitness.
- Hitchhiking effect
This occurs when a neutral mutation is in linkage disequilibrium with a second locus that is undergoing a selective sweep.
- Long-branch attraction
The phenomenon of inferring an incorrect phylogenetic tree owing to the presence of sequences that evolve rapidly and generate long branches that are mispositioned — usually attracted to the base — and thus distort the tree.
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Albalat, R., Cañestro, C. Evolution by gene loss. Nat Rev Genet 17, 379–391 (2016). https://doi.org/10.1038/nrg.2016.39
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