Extended Synthesis and future perspectives

Despite the efficacy of the Modern synthesis in describing the genetic implications of evolution, further advances were made in the last 20 years and exceptions to the basic assumptions of the MS were identified. These exceptions raised the question of whether these basic assumptions should be revisited or whether additional drivers should be simply added (Wilkins 2008; Laland et al. 2015). Following these findings and this line of reasoning Massimo Pigliucci and Gerd B. Müller postulated a new “Extended Evolutionary Synthesis” (EES; Müller 2007; Pigliucci 2009). This consists of revisiting the basic assumptions of the ES by giving more importance to the role of phenotypes and including additional evolutionary processes, as described in Table 1. The basic assumptions of the EES embrace and extend the ones of the ES. The three main EES assumptions are listed below (for mor details see Laland et al. 2015):

1. Inclusive inheritance: Genetic mutations but also other forms of inheritance generate variation.

2. Reciprocal causation: Evolutionary processes cause phenotypic variation in the new generations but vice versa the phenotypes influence the occurrence of evolutionary processes.

3. Non-random variation: There is evidence that variation is not generated fully randomly. One controversial example is “developmental bias” , referring to the observation that some phenotypes are more likely than others to arise due to developmental processes. Moreover, it was shown that, responding to specific stimuli, extra chromosomal DNA molecules can be replicated to create redundancy of beneficial genes. This mechanism was shown to induce glyphosate resistance in Amaranthus palmeri and constitutes another striking example of non-random genetic variation . Again, some families of transposable elements seem to be preferentially inserted in the proximity of genes and not fully randomly in the genome . Environmentally induced epigenetic variation, if stable through at least few generations, would constitute another case of non-random variation.

Table 1: Evolutionary processes considered by the Extended Evolutionary Synthesis as described in Laland et al. 2015.

EES evolutionary processes	Definition and explanation
Developmental bias	This refers to the discovery that developmental processes can affect phenotypic variation as some phenotypic forms are more likely to arise than others. For example, the number of limbs, digits, segments and vertebrae across a variety of taxa is non-random, due to developmental processes specifically propending to create specific numbers of these modular structures.
Developmental plasticity	Plasticity facilitates novel environment colonisation by species and could influence evolution by affecting population connectivity and gene flow and exposing populations to different selective pressures and therefore increasing the chance of adaptive peak shifts.
Inclusive inheritance	Inclusive inheritance considers that the progeny does not only inherit the genetic information from the parents, but also several other information such as transgenerational epigenetic marks and several kinds of parental effects such as egg components, post fertilization resources , symbionts, parental modification of the environment and social behaviour/knowledge. Human societies are an example of this process, as we would never have evolved to our current state without inheriting knowledge and social behaviour from the previous generations.
Niche construction	Niche construction refers to the ability of a species to modify the surrounding environment, affecting the selective pressures acting on itself and, in some cases, even other species . The most straightforward example is in human evolution, as we are able to extensively modify our surrounding environment, erasing many of the selective pressures acting on our species.
Genetic accommodation	Genetic accommodation refers to genetic modifications “fixing” a character previously provided only by plasticity. When plasticity allows a population to colonise a new environment, this will also expose it to a new selection of standing or new genetic variation. This is the main process used by the EES to explain how phenotypes, developmental bias, plasticity … can play a role in evolution.

Despite the evident effect of some of the EES additional drivers (especially when thinking about human evolution), some authors argue that these additional drivers are only affecting evolution indirectly and they introduce variation that can be already captured by the original drivers (Futuyma 2017). To give real life examples, it is possible to explain humans loss of body hairs as a result of niche construction, removing the selective pressure (cold protection) or to explain it directly with the loss of the selective pressure for that trait. In the same manner, genetic divergence between populations can be explained as the result genetic accommodation following colonization events only provided by plasticity, or directly as the result of different populations being exposed to different selective pressures.

Without getting into the details of such discussion, it is important to point out that transgenerational epigenetics, referring to epigenetic marks stably inherited through generations, when having a phenotypic effect, would be directly influencing evolution and not in an indirect way like other EES mechanisms. For this reason, in this chapter we will primarily focus on stable epigenetic variation (see “Stability of Epigentic marks”). The concept of “stable” strictly depends on the mode of reproduction of the species, hence in asexually reproducing species mitosis-heritable epigenetic marks should be considered stable, while stability through meiosis would be necessary for sexually reproducing species.

This considered, transgenerational epigenetics is one of the most prominent candidates to be included in new evolutionary models. Nevertheless, according to Occam’s razor, a good model should be simple, and the question of whether or not transgenerational epigenetics would significantly increase the accuracy and power of the evolutionary theory is still under debate (Dickins and Barton 2013; Haig 2007; Pigliucci and Finkelman 2014; Mesoudi et al. 2013). It is therefore crucial to determine the relative contribution of epigenetics to evolution, in order to implement it correctly in future evolutionary models.