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Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning

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Abstract

Traditional accounts of the role of learning in evolution have concentrated upon its capacity as a source of fitness to individuals. In this paper I use a case study from invasive species biology—the role of conditioned taste aversion in mitigating the impact of cane toads on the native species of Northern Australia—to highlight a role for learning beyond this—as a source of evolvability to populations. This has two benefits. First, it highlights an otherwise under-appreciated role for learning in evolution that does not rely on social learning as an inheritance channel nor “special” evolutionary processes such as genetic accommodation (both of which many are skeptical about). Second, and more significantly, it makes clear important and interesting parallels between learning and exploratory behaviour in development. These parallels motivate the applicability of results from existing research into learning and learning evolution to our understanding the evolution of evolvability more generally.

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Notes

  1. There are exceptions to this general rule. A small number of native species have been observed to be relatively “immune” to toad toxin (e.g. the keelback snake, Tropidonophis mairii). The “preadaptation” to toads in these lineages is believed to be the product of contact between ancestors of these native species and Bufonid toads in Asia (where such species are endemic) prior to migration onto the Australian continent (Llewelyn et al. 2010a, 2011).

  2. Note, red-bellied black snakes are not incapable of learning full stop, they simply do not exhibit learning with respect to cane toads (Phillips and Shine 2006).

  3. It is important to note that this claim—that learning influences evolvability—is made elsewhere (albeit in passing) within the literature on the contribution of adaptive phenotypic plasticity to the evolvability of populations (in particular, see Pfennig et al. (2010); West-Eberhard (2003); Fitzpatrick (2012)) and also that concerning the Baldwin effect (e.g., Papineau 2005). Here, I am both making the claim regarding learning clearer and more specific but also, as will become apparent, highlighting some novel implications for evolutionary developmental biology.

  4. Note that, although there are documented cases of relatively large, but genetically homogeneous, populations, such populations are rare and fragile. To illustrate, prior to 2008, Tasmanian devil (Sarcophilus harrisii) populations in Tasmania were very large, but exhibited low levels of genetic diversity at a number of particularly polymorphic parts of the mammalian genome (McCallum 2008). Therefore, this population lacked robustness. Since 2008, devil populations have been decimated by a particularly virulent host-specific pathogen whose transmission is aided by the genetic homogeneity of the devil population. Because of the fragility of populations like this (and thus their rarity), it is a relatively uncontroversial assumption of much of conservation biology that small populations have lower standing genetic variation than larger ones (Boyce 1992; Shaffer 1981).

  5. There is considerable conceptual confusion surrounding the term "robustness" both within the sciences and in the philosophy of science (Wimsatt 2007) but also more specifically in evolutionary developmental biology (this confusion concerns relationship between robustness and evolvability—see Wagner 2005; Wagner 2008; Lenski et al. 2006; Brookfield 2009). As such, note that here I mean “robustness” to refer to the ability of a population or lineage to respond adaptively to environmental change. I take it that, at least with respect to a population’s capacity to evolve adaptation (i.e., their evolvability with respect to adaptation), this type of robustness is not in conflict with evolvability. A population that is robust in this manner is also evolvable with respect to complex adaptation.

  6. Unfortunately, I was unable to find any data in the literature on the genetic diversity of red-bellied black snake and planigale populations that I could use to test the hypotheses I make here.

  7. There are certain situations (e.g., chimerism) in which there can be divergence in the interests of the cells within the body but these are rare.

  8. I was able to find some research that is at least related. In birds there is evidence that there is no link between behavioural flexibility and extinction risk (Nicolakakis et al. 2003). Behavioural flexibility and asocial learning are not strictly the same thing, however, though the former may be necessary for the latter. It would be interesting to see if there was a relationship between behavioural flexibility and extinction risk when coupled with asocial learning.

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Acknowledgments

I am particularly grateful to Kevin Laland for his detailed comments and encouragement on the material in this paper. I would also like to acknowledge Brett Calcott, Ellen Clarke and Kim Sterelny along with audiences at the Australian National University and the 2011 Philosophy of Biology at Dolphin Beach Workshop in Moruya, NSW for their comments on earlier iterations the work. Funding for this research was provided through the generous support of an Australian National University PhD scholarship and a writing-up fellowship at the Konrad Lorenz Institute for Evolution and Cognition Research in Altenberg, Austria.

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  1. School of Philosophy and Centre for Macroevolution and Macroecology: Tempo and Mode, Australian National University, Canberra, ACT, 0200, Australia

    Rachael L. Brown

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Brown, R.L. Learning, evolvability and exploratory behaviour: extending the evolutionary reach of learning. Biol Philos 28, 933–955 (2013). https://doi.org/10.1007/s10539-013-9396-9

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