Since 1892, it has been widely assumed that somatic mutations are evolutionarily irrelevant in animals because they cannot be inherited by offspring; in some corals they found inheritance of somatic mutations

Kate L. Vasquez Kuntz, Sheila A. Kitchen, Trinity L. Conn, Samuel A. Vohsen, Andrea N. Chan, Mark J. A. Vermeij, Christopher Page, Kristen L. Marhaver, Iliana B. Baums. Inheritance of somatic mutations by animal offspring. Science Advances, 2022; 8 (35) DOI: 10.1126/sciadv.abn0707

Abstract: Since 1892, it has been widely assumed that somatic mutations are evolutionarily irrelevant in animals because they cannot be inherited by offspring. However, some nonbilaterians segregate the soma and germline late in development or never, leaving the evolutionary fate of their somatic mutations unknown. By investigating uni- and biparental reproduction in the coral Acropora palmata (Cnidaria, Anthozoa), we found that uniparental, meiotic offspring harbored 50% of the 268 somatic mutations present in their parent. Thus, somatic mutations accumulated in adult coral animals, entered the germline, and were passed on to swimming larvae that grew into healthy juvenile corals. In this way, somatic mutations can increase allelic diversity and facilitate adaptation across habitats and generations in animals.

Popular version: Corals pass mutations acquired during their lifetimes to offspring. August 31, 2022. https://www.sciencedaily.com/releases/2022/08/220831152728.htm

DISCUSSION

By investigating uniparental and biparental, meiotic offspring from the coral A. palmata, we show that somatic mutations at multiple loci, which were acquired over the lifetime of a parent animal, can be inherited by its offspring (Figs. 1 and 2 and fig. S7). These findings were reproducible across two spawning years and in two locations at opposite ends of the species’ range (note S5). Because coral genets can persist for hundreds to thousands of years, somatic mutations can rise to high frequency in modules (polyps) of a genet due to stochasticity or selection (35, 36). Strongly deleterious or lethal mutations might lead to module or colony death, but not genet death, and can thus be removed from the genet’s gene pool while preserving the genet itself. Meanwhile, neutral and beneficial somatic mutations can accumulate in tissues, spread to new modules via polyp budding, and be dispersed over small spatial scales through colony fragmentation [ca. 70 m, (37)]. After these mutations are inherited by offspring, fitness variance is redistributed from the realm of within-colony to between-organism selection. Furthermore, these somatic mutations have the potential to disperse over much longer distances [hundreds of kilometers, (38)] by pelagic coral larvae that have inherited the mutations. Thus, the discovery of heritable somatic mutations in coral offspring represents a previously unconfirmed source for coral adaptation and evolution.

The mechanism by which adult A. palmata transmit somatic mutations to offspring remains to be found (Fig. 4). Mutations may have originated in the soma, dedifferentiated into stem cells, and then redifferentiated into germ cells, or somatic cells may have transdifferentiated directly into germ cells (39). Stem cells have not yet been identified in corals; however, the regenerative properties of anthozoans (40, 41) and the identification of progenitor/undifferentiated cells with stem cell characteristics in a sea anemone (42) and in coral cell lines (43) both point to their existence (19, 35). In any case, the mutations identified and tracked in this study must have occurred after embryogenesis of the primary polyp that founded the genet was complete because the mutations were not shared among all polyps of the adult parent genet or all ramets of the genet. This implies that multipotent progenitor or stem-like cells are not moving freely throughout a colony, setting up competition among cells of different stem cell lineages.

[Fig. 4. Modes of inheritance of genetic mutations in animals.

(1) If animals differentiate and segregate germline cells (light blue) from somatic cells (light orange) early in development, then only germline mutations (medium blue) can be inherited by offspring (1). (2) Planarians, sponges, and some cnidarians continuously segregate a germline and somatic tissue from a population of stem cells (brown) as they grow, allowing for an accumulation of mutations that are heritable (11). (3) Cnidarian somatic cells may de- or transdifferentiate into germline cells, passing on mutations that are somatic in origin (dark blue) (14). The cellular source (soma, germ, or stem) for polyp growth is an active area of research. (4) Somatic mutations (dark orange) may rise to fixation in new modules (polyps) through budding from a limited number of soma cells. Lightning bolts represent mutation-causing events. Figure modified with permission from Reusch et al. (21).]

Immediately after a somatic cell mutates, it undergoes competition with nonmutated cells in a process called developmental selection (36, 44–46). This “struggle of the parts,” as described by Wilhelm Roux in 1881 and later recognized by Weismann as “intraorganismal selection,” is distinct from germline selection (47, 48) and can occur at the molecular, chromosome, or cellular level. Propagation of the somatic mutation then depends on either successfully outcompeting or coexisting with other somatic lineages during cell growth and proliferation (21, 49). Beneficial (or neutral) mutations that survive developmental selection can therefore be disproportionately represented in the cells of a genet (50), an advantage that germline mutations do not have. Somatic mutations with beneficial fitness effects in clonal organisms may be more common than previously thought (51, 52) and may allow ramets to withstand environmental fluctuations. Here, we show that gametes carrying somatic mutations survive to form healthy juvenile corals.

A high percentage of the coral offspring analyzed here were uniparental (73%) compared to previous studies [~1 to 10% uniparental offspring; (53, 54)]. While this is not common in animals nor is it typical for most broadcast spawning corals, uniparental reproduction is common in plants. Plant species frequently switch from biparental to uniparental reproduction when sexual partners are scarce, e.g., at the edges of the species range, when introduced to new habitats, or after large-scale disturbances (55, 56). Hence, like plants, corals may rely on the generation of uniparental larvae to persist during times when sexual partners are rare. Within-genet selection before gametogenesis may effectively purge lethal recessive mutations that would otherwise be exposed to selection only during mating between genets and so reduce the cost of selfing/uniparental inheritance (36, 57). Thus, the production of uniparental offspring that harbor parental somatic mutations might help buffer against the losses of genetic diversity and consequences of inbreeding (56) that would otherwise occur in uniparental mating, i.e., as a result of self-fertilization (32).

Modular species are found in multiple groups (e.g., multicellular algae, fungi, and animals) across the eukaryotic tree of life (21), and a small number of researchers have suggested that somatically generated variation should be considered to understand evolution in these taxa (36, 58). However, the common assumption that Weismann’s barrier is universal in animals (7) has led biologists to disregard somatic mutations as a potentially important source of new genetic variation to shape animal evolution. Our demonstration of transgenerational inheritance of acquired genetic variation challenges this long-held assumption. Like many other modular, long-lived marine invertebrates, terrestrial plants, and even seagrasses, coral genets experience substantial environmental pressures over their long life spans, and somatic mutations may play a major role in their adaptation to these changes (21, 59). Our findings further illustrate the narrowing differences known to exist in the evolutionary dynamics characterizing plants and nonbilaterian animal groups such as corals.