Abstract
Recent work on inheritance systems can be divided into inclusive conceptions, according to which genetic and non-genetic inheritance are both involved in the development and transmission of nearly all animal behavioral traits, and more demanding conceptions of what it takes for non-genetic resources involved in development to qualify as a distinct inheritance system. It might be thought that, if a more stringent conception is adopted, homologies could not subsist across two distinct inheritance systems. Indeed, it is commonly assumed that homology relations cannot survive a shift between genetic and cultural inheritance systems, and substantial reliance has been placed on that assumption in debates over the phylogenetic origins of hominin behavioral traits, such as male-initiated intergroup aggression. However, in the homology literature it is widely accepted that a trait can be homologous—that is, inherited continuously in two different lineages from a single common ancestor—despite divergence in the mechanisms involved in the trait’s development in the two lineages. In this paper, we argue that even on an extremely stringent understanding of what it takes for developmental resources to form a separate inheritance system, homologies can nonetheless subsist across shifts between distinct inheritance systems. We argue that this result is a merit of this way of characterizing what it is to be an inheritance system, that it has implications for adjudicating between alternative accounts of homology, and that it offers an important cautionary lesson about how (not) to reason with the homology concept, particularly in the context of cultural species.
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Notes
This paper does not take a stand on the general ‘problem of homology.’ Instead, we will simply stipulate that by ‘homology’ we mean ‘taxic homology’ which we define, broadly following Wiley and Lieberman (2011), as ‘character states that are shared by two taxa and inherited continuously from their common ancestor’. In contrast, ‘homoplasy’ will refer to qualitatively similar character states that do not stem from a common ancestor (and hence diagnose polyphyletic groups). Our focus is therefore on the homology of similar character states, rather than on individuated characters whatever their state.
We use the term ‘phenotype’ in the broad, ‘extended’ sense to include not only quintessential biological structures but also behaviors, mental representations, and artifacts.
Animal taxa have been subject to a non-trivial amount of lateral gene exchange mediated by viral vectors (Keeling and Palmer 2008), and hybridization between disparate plant species may occur at an evolutionarily significant frequency, but these phenomena are not substantial enough to undermine the project of using DNA to build phylogenetic trees in eukaryotes.
If there has been selection for mechanisms that stabilise membrane-based inheritance over and above stabilising the integrity of membranes in ontogeny, then it would qualify as a (limited) inheritance system.
Some inheritance systems may have been selected to have medium fidelity of transmission, with the function of transmitting phenotypes down multiple generations, but many fewer generations than are usually involved in genetic transmission.
That there is cultural heritability does not entail that there is a cultural inheritance system, on our more stringent account of the latter. A particular culturally copied phenotype can confer a fitness advantage on individuals or groups without culture being a system that is itself selected for transmitting adaptive variation down the generations.
‘Cultural assimilation’ in the sense used here is to be distinguished from the scenario wherein a trait not transmitted by any inheritance system (e.g., an individually learned trait) comes to be culturally transmitted. The process just described, which is arguably common in cultural evolution (Gers 2011), is a cultural analog of genetic assimilation, but not one that would involve the shift across inheritance systems that we contemplate in this paper. Note that if one takes a broader view of cultural assimilation such that it includes the cultural cooptation and transmission of individually learned behaviors, then the process of cultural assimilation need not begin with a genetic mutation or innovation.
Further complications arise due to the fact that selection on conserved developmental mechanisms can result in the repeated origination (and loss) of a trait in a bushy clade (i.e., ‘parallelism’)—which one may (Ramsey and Peterson 2012) or may not (Currie 2013) prefer to categorize as homologs. Furthermore, one might think that behavioural traits, such as intergroup hostility, will be especially prone to iterated evolution, given that they are labile, only loosely tied to structure, and partly functionally delineated. In fact, insofar as this lability entails greater degrees of freedom in alternative character state space, the phylogenetic signal of behaviors and culturally acquired traits will be less prone to homoplastic noise (Rendall and Di Fiore 2007). In any case, these are epistemic difficulties that confront the homologization of behavioral characters in general, not simply those implicating cultural traits or shifts across inheritance systems. A full treatment of these important issues lies beyond the scope of the present discussion.
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Acknowledgments
We would like to thank Gerd Müller, Grant Ramsey, Louise Roth, Tobias Uller, Günter Wagner, and two anonymous reviewers for helpful comments on an earlier draft of this manuscript. Russell Powell would like to thank the Konrad Lorenz Institute for Evolution and Cognition Research, as well as the Templeton Foundation Grant #43160, for support of this research.
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Powell, R., Shea, N. Homology across inheritance systems. Biol Philos 29, 781–806 (2014). https://doi.org/10.1007/s10539-014-9433-3
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DOI: https://doi.org/10.1007/s10539-014-9433-3