Philosophy of Biology and Cognitive Sciences

Evolvability is the capacity of populations to evolve or produce heritable phenotypic variation. Accordingly, understanding evolvability involves an interrogation about sources of phenotypic novelty (Kirschner and Gerhart 1998, Kirschner 2013). Evolvability is seen as an ability facilitating the evolution of populations, and, within the framework of evo-devo, this ability is deeply rooted in developmental features such as modularity and robustness (Wagner and Altenberg 1996). Nevertheless, for development to contribute to evolvability a further linkage with evolution is required. Evolutionary change not only depends on developmental factors; it also relies on explanatory causes
involving environmental influences. This means that variation not only needs to be phenotypically translated, but it also must lead to viable results with significant probability. For example, as evolvability relies on how the architecture of development, or the genotype-phenotype map (GPM), is organized, modularity, as a variational property reducing pleiotropic deleterious and redundant effects, is expected to promote evolutionary change (Wagner 1995, 1996). However, typical evo-devo approaches to evolvability, in identifying developmental and embryonic properties, have overlooked those developmental relations taking place between different organisms or in transitions
to new levels of individuality. I will argue instead that seeing evolvability through the lenses of broader developmental interactions can also shed light on this necessary capacity of living beings.

 

In this paper, I will look at a case study where evolvability can be characterized with reference to morphological burst in a given lineage over evolutionary time. The marsupial/eutherian split will be my case study to explore this hypothesis, as marsupials only display 5% of eutherian taxonomic diversity (Walke 1999). We will refer to how modularity might be a central condition for evolvability in
this case. The concept of modularity assumes that complex organisms are formed by structural, physiological and developmental units that are relatively autonomous in term of genetic specification, can evolve independently and exist at different levels of biological organization. However, although modular organisms are usually theorized along with the issue of biological individuation, and a distinction between reproductive and non-reproductive modules is gradually starting to emerge (Winther 2001), the problem of modularization has not yet been related to mother/fetus interactions during pregnancy. This is especially relevant since slower reproductive processes, as it is the case of mammalian pregnancy, as well as a lower number of offspring, have sometimes been conceptually linked to lower evolvability in those conceptualizations of maternal influence as an environmental niche of the embryo (Dupré 2017). For this reason, I will look at the modularization of the reproductive relation between mother and embryos, instead of restricting variational properties to intraembryonic structures. I will argue that including reproductive, developmental relations in the issue of modularity entails an association of variational modularity with the semi-autonomous status of two different organisms. The disparity in the degree of anatomical experimentation between marsupial and eutherians very much results from their distinct reproductive, adaptive strategies.

 

Nonetheless, the developmental mechanisms involved in each type of pregnancy have tended to be neglected. In eutherian mammals, some of these include the evolution of extra-embryonic membranes associated with ancestrally invasive placentation and the origin of a new cell type (the decidual cell) resulting from an extensive interaction between trophoblast and endometrial cells (Wagner et al. 2014). I hypothesize that these developmental innovations on the extraembryonic side have enhanced evolvability among eutherian mammals by increasing embryo organogenesis independence over ontogenetic and evolutionary scales. In marsupials, the degree of evolvability is limited toward a restricted number of morphological end-states, given that the marsupial newborn requires reaching the nipple in an altricial state of maturation. In eutherians, however, morphological adaptations to different environments (such as direct development to fully aquatic species) and a broader manifestation of adaptive phenotypes were enabled (Lillegraven 1974). Having this case study in mind, I will reflect on the relationship between development, reproduction, and evolvability to consider how a broader range of types of variation can be an indicator of evolvability within the evo-devo paradigm. This contradicts the concept of evolvability in terms of population dynamics, wherein heritability of variation is regarded quantitatively without attending to how many new morphological end-states come up, and differential reproduction is the crucial result. Accordingly, the ease with which a lineage can move through the morphological space without compromising viability is seen here from a viewpoint that focuses on reproductive relations and does not reduce its role to the differential survival of self-replicating entities. To conclude, I argue that the marsupial/eutherian split illustrates how developmental innovations related to pregnancy might have influenced evolvability.

 

References
Dupré, J. (2017). The metaphysics of evolution. Interface focus, 7(5), 20160148.
Kirschner, M., & Gerhart, J. (1998). Evolvability. Proceedings of the National Academy of Sciences, 95(15), 8420-8427.
Kirschner, M. (2013). Beyond Darwin: evolvability and the generation of novelty. BMC biology, 11(1), 110.
Lillegraven, J. A. (1975). Biological considerations of the marsupial‐placental dichotomy. Evolution, 29(4), 707-722.
Nowak, R. M., & Walker, E. P. (1999). Walker's Mammals of the World (Vol. 1). JHU Press.
Wagner, G. P. (1995, June). Adaptation and the modular design of organisms. In European Conference on Artificial Life (pp. 315-328). Springer, Berlin, Heidelberg.
Wagner, G. P. (1996). Homologues, natural kinds and the evolution of modularity. American Zoologist, 36(1), 36-43.
Wagner, G. P., & Altenberg, L. (1996). Complex Adaptations and the Evolution of Evolvability. Evolution, 50, 967-976.
Wagner, G. P., Kin, K., Muglia, L., & Pavličev, M. (2014). Evolution of mammalian pregnancy and the origin of the decidual stromal cell. International Journal of Developmental Biology, 58(2-3-4), 117-126.
Winther, R. G. (2001). Varieties of modules: kinds, levels, origins, and behaviors. Journal of Experimental Zoology, 291(2), 116-129.