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Review
. 2024 Oct 16:12:1453566.
doi: 10.3389/fcell.2024.1453566. eCollection 2024.

Developmental bias as a cause and consequence of adaptive radiation and divergence

Corin Stansfield  1 , Kevin J Parsons  1
Affiliations
Review

Developmental bias as a cause and consequence of adaptive radiation and divergence

Corin Stansfield et al. Front Cell Dev Biol. .

Abstract

Efforts to reconcile development and evolution have demonstrated that development is biased, with phenotypic variation being more readily produced in certain directions. However, how this "developmental bias" can influence micro- and macroevolution is poorly understood. In this review, we demonstrate that defining features of adaptive radiations suggest a role for developmental bias in driving adaptive divergence. These features are i) common ancestry of developmental systems; ii) rapid evolution along evolutionary "lines of least resistance;" iii) the subsequent repeated and parallel evolution of ecotypes; and iv) evolutionary change "led" by biased phenotypic plasticity upon exposure to novel environments. Drawing on empirical and theoretical data, we highlight the reciprocal relationship between development and selection as a key driver of evolutionary change, with development biasing what variation is exposed to selection, and selection acting to mold these biases to align with the adaptive landscape. Our central thesis is that developmental biases are both the causes and consequences of adaptive radiation and divergence. We argue throughout that incorporating development and developmental bias into our thinking can help to explain the exaggerated rate and scale of evolutionary processes that characterize adaptive radiations, and that this can be best achieved by using an eco-evo-devo framework incorporating evolutionary biology, development, and ecology. Such a research program would demonstrate that development is not merely a force that imposes constraints on evolution, but rather directs and is directed by evolutionary forces. We round out this review by highlighting key gaps in our understanding and suggest further research programs that can help to resolve these issues.

Keywords: eco-evo-devo; ecotype evolution; evolvability; extended evolutionary synthesis; parallel evolution; phenotypic plasticity; plasticity-led evolution; quantitative genetics.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Defining features of adaptive radiations suggest a role for developmental bias. (A) If lines of least resistance align with axes of selection, evolution can be greatly accelerated. Cichlid speciation (left) and sequence divergence is rapid, surpassing neutral expectations, and evolutionary rates in a non-radiating family, Sebastes rockfish. Figure from Schluter (2000) p.15. (B) Evolution tends to follow “lines of least resistance.” Rhoda et al. (2023) found that ruminant cranial evolution follows a line of least resistance driven by an allometric relationship between face length and cranium size. Thus, variation is restricted to a narrower region of phenotypic space (blue) than would be expected under the null hypothesis of isotropic variation (grey). (C) Similar patterns of developmental bias within a lineage can contribute to parallel evolution. Many similar species have emerged independently in three African Rift Lakes - Malawi, Victoria and Tanganyika. Diagram from Stiassny and Meyer (1999) shows fish from lake Tanganyika on the left, and similar varieties from Lake Malawi on the right. (D) Adaptive radiation is characterised by ecotypic divergence, driven by altered patterns of covariation. Galapagos finches represent a textbook example, due to divergence in skull and beak morphology in response to different feeding niches. Figure from Mallarino et al. (2011). (E) The Anolis adaptive radiation is characterised by the repeated emergence of six ecotypes, inhabiting different microhabitats. Figure from Huie et al. (2021) (F) Adaptive radiation are often facilitated by “key innovations,” seeded through altered patterns of covariation that bias evolution towards certain regions of phenotypic space. Drake and Klingenberg (2010) demonstrated that the canine skull is composed of two modules, mandibular (black) and cranial (white), and associated this developmental lability with the diversity observed within domestic dog breeds, which eclipses that of the entire carnivora family. (G) Adaptive divergence is often seeded through phenotypic plasticity, which is biased in nature. Wund et al. (2008) demonstrated that specialised benthic and limnetic feeding morphologies (bottom), characterised by patterns of covariaton, could be recapitulated plastically in the marine ancestor (top). Such “plasticity-led evolution” is a characteristic feature of adaptive radiations.
FIGURE 2
FIGURE 2
Bias as a cause and consequence of adaptive radiations and divergence. (A) Common ancestry may lead to similarly-biased developmental systems. As a result, parallel evolution may be more likely within a lineage, or one lineages may be able to evolve in the face of ecological “opportunity” while another lineage cannot. (B) Evolution tends to occur along “lines of least resistance,” captured by Gmax – the axis along which the most additive genetic variation is produced. If Gmax aligns with the fitness landscape (θ is small), then adaptive evolution may by accelerated (e.g., θ1). Conversely, if Gmax for a population or lineage is not aligned with the fitness landscape (θ is large, e.g., θ2) adaptation may be slowed or constrained entirely. Hence, biases can be viewed as permissive and constraining forces. (C) Lines of least resistance typically correlate with multiple ecotypes. For example, Schluter’s (1996) line of least resistance for threespine stickleback contained slender, shallow-bodies limnetic forms at one end and deep-bodied limnetic forms at the other end. (D) Parallel evolution of ecotypes can occur through a combination of parallel selection pressures and parallel patterns of bias. Benthic-limnetic divergence has occurred numerous times independently in sticklebacks, as has the emergence of similar divergent phenotypes in response to different environmental gradients. (E) Adaptive divergence results in altered patterns of developmental bias. Thus, biases can be viewed as consequences, as well as causes, of adaptive divergence and radiation. Future evolution can be accelerated if it occurs along axes previously favoured by selection. (F) Rapid evolution can occur via biased phenotypic plasticity. “Learning” can occur in gene regulatory networks, allowing rapid plastic switching between ecotypic forms that can become refined over time (hard arrows). Developmental noise induced by novel environmental cues will further be directed along axes previously favoured by selection (dashed arrows).
FIGURE 3
FIGURE 3
Reciprocity between development and selection drives evolution. Development influences selection by “biasing” the phenotypic variation that is made available (top arrow). When selection acts on phenotypic variation, it is also acting the developmental processes that generate said variation. Hence developmental biases can confer evolvability, and this evolvability is under selection and thus capable of evolving (bottom arrow). By acting on developmental processes and evolvability, selection influences the distribution of phenotypic variation in the next generation, thus what variation is exposed to selection.
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Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by the BBSRC grant number X010902/1 awarded to CS.

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