Bayesian inference of ancestral host-parasite interactions under a phylogenetic model of host repertoire evolution

Abstract

Intimate ecological interactions, such as those between parasites and their hosts, may persist 1 over long time spans, coupling the evolutionary histories of the lineages involved. Most methods that 2 reconstruct the coevolutionary history of such associations make the simplifying assumption that parasites 3 have a single host. Many methods also focus on congruence between host and parasite phylogenies, using 4 cospeciation as the null model. However, there is an increasing body of evidence suggesting that the host 5 ranges of parasites are more complex: that host ranges often include more than one host and evolve via 6 gains and losses of hosts rather than through cospeciation alone. Here, we develop a Bayesian approach for 7 inferring coevolutionary history based on a model accommodating these complexities. Specifically, a 8 parasite is assumed to have a host repertoire, which includes both potential hosts and one or more actual 9 hosts. Over time, potential hosts can be added or lost, and potential hosts can develop into actual hosts or 10 vice versa. Thus, host colonization is modeled as a two-step process, which may potentially be influenced 11 by host relatedness or host traits. We first explore the statistical behavior of our model by simulating 12 evolution of host-parasite interactions under a range of parameters. We then use our approach, 13 implemented in the program RevBayes, to infer the coevolutionary history between 34 Nymphalini 14 butterfly species and 25 angiosperm families. 15(Keywords: ancestral hosts, coevolution, herbivorous insects, probabilistic modeling.) 16 Extant ecological interactions, such as those between parasites and hosts, are often the 17 result of a long history of coevolution between the involved lineages (Elton 1946; Klassen 1992). 18 Specialization is predominant among parasites (including parasitic herbivorous insects; Forister 19 et al. 2015), but host associations are not static: they continuously evolve over time via gains and 20 losses of hosts (Janz and Nylin 2008; Nylin et al. 2018). The colonization of new hosts and loss of 21 old hosts not only shape the evolutionary trajectories of the interacting lineages, but can also 22 have large effects at ecological timescales (Nosil 2002; Calatayud et al. 2016). These effects are 23 evident, for example, with emerging infectious diseases and zoonotic diseases (Acha and Szyfres 24 2003), which involve colonization of new hosts within and among groups of domesticated species 25 (Subbarao et al. 1998), wildlife (Fisher et al. 2009), and humans (Hahn et al. 2000). Unraveling 26 the processes underlying changes in species associations is thus key to understanding evolutionary 27and ecological phenomena at various timescales, such as the emergence of infectious diseases, 28 community assembly, and parasite diversification (Hoberg and Brooks 2015). 29Many methods developed to study historical associations focus on congruence between 30 host and parasite phylogenies (Brooks 1979; Huelsenbeck et al. 1997; de Vienne et al. 2013). S...

Universal probabilistic programming offers a powerful approach to statistical phylogenetics

“…Separately, we show how PPLs can be applied to models where diversification rates are dependent on observable traits of organisms (so-called state-dependent speciation and extinction models) 37 . Other problem domains that may benefit from the PPL approach already at this point include epidemiology 45 , host-parasite co-evolution 46 , and biogeography 47,48,49,50 .…”

The ghost of hosts past: impacts of host extinction on parasite specificity

“…Predictions of unobserved host–parasite associations are often based on an assumption that present-day associations accurately reflect potential host ranges [ 31 , 35 , 36 ]. However, host range is a dynamic property of parasites that evolves through cospeciation, host shifts, and the gains and losses of hosts over varying timescales [ 37 – 41 ]. Changes in parasite host specificity as a result of host-switching and shifting geographic ranges have attracted considerable attention by researchers [ 42 – 47 ], whereas extinction history has tended to be overlooked.…”

The role of phylogeny and ecological opportunity in host-parasite interactions: network metrics, host repertoire, and network link prediction.

“…after anthropogenic introductions (Brookset al 2021). Therefore, the realised host repertoire , which is approximated through FPDist, does not equate the full repertoire of host species that can potentially be infected (fundamental host repertoire ) (Braga et al 2020). The oscillation of host ranges resulting from ecological fitting and opportunity has been termed the Stockholm Paradigm (Brookset al 2019) and is considered one of the main sources of parasite biodiversity (Agosta & Brooks 2020).…”