A niche perspective on the range expansion of symbionts

Abstract

Range expansion results from complex eco‐evolutionary processes where range dynamics and niche shifts interact in a novel physical space and/or environment, with scale playing a major role. Obligate symbionts (i.e. organisms permanently living on hosts) differ from free‐living organisms in that they depend on strong biotic interactions with their hosts which alter their niche and spatial dynamics. A symbiotic lifestyle modifies organism–environment relationships across levels of organisation, from individuals to geographical ranges. These changes influence how symbionts experience colonisation and, by extension, range expansion. Here, we investigate the potential implications of a symbiotic lifestyle on range expansion capacity. We present a unified conceptual overview on range expansion of symbionts that integrates concepts grounded in niche and metapopulation theories. Overall, we explain how niche‐driven and dispersal‐driven processes govern symbiont range dynamics through their interaction across scales, from host switching to geographical range shifts. First, we describe a background framework for range dynamics based on metapopulation concepts applied to symbiont organisation levels. Then, we integrate metapopulation processes operating in the physical space with niche dynamics grounded in the environmental arena. For this purpose, we provide a definition of the biotope (i.e. living place) specific to symbionts as a hinge concept to link the physical and environmental spaces, wherein the biotope unit is a metapopulation patch (either a host individual or a land fragment). Further, we highlight the dual nature of the symbionts' niche, which is characterised by both host traits and the external environment, and define proper conceptual variants to provide a meaningful unification of niche, biotope and symbiont organisation levels. We also explore variation across systems in the relative relevance of both external environment and host traits to the symbiont's niche and their potential implications on range expansion. We describe in detail the potential mechanisms by which hosts, through their function as biotopes, could influence how some symbionts expand their range – depending on the life history and traits of both associates. From the spatial point of view, hosts can extend symbiont dispersal range via host‐mediated dispersal, although the requirement for among‐host dispersal can challenge symbiont range expansion. From the niche point of view, homeostatic properties of host bodies may allow symbiont populations to become insensitive to off‐host environmental gradients during host‐mediated dispersal. These two potential benefits of the symbiont–host interaction can enhance symbiont range expansion capacity. On the other hand, the central role of hosts governing the symbiont niche makes symbionts strongly dependent on the availability of suitable hosts. Thus, environmental, dispersal and biotic barriers faced by suitable hosts apply also to the symbiont, unless eventual opportunities for host switch...

Positive species interactions shape species' range limits

“…More specifically, we assess how much evidence there is that positive interactions play a significant role in defining range limits or impact range expansion processes, and we address the extent to which the effects of positive interactions vary across interaction types. Inspired by previous theory on this topic (Bruno et al 2003, Sexton et al 2009, HilleRisLambers et al 2013, Bulleri et al 2016, Mestre et al 2020, we hypothesise that while 1) facultative interactions tend to extend species' ranges (Fig. 1F, 2) obligate interactions generally constrain ranges (Fig.…”

Animal migrations and parasitism: reciprocal effects within a unified framework

“…Second, host-mediated dispersal across large geographic scales means that parasites of migrants should on average be exposed to a broader range of alternative host species than parasites of non-migrants, which should favour a relaxation of host specificity and facilitate host-switching. Host migration provides repeated re-introduction to an area and sustained propagule pressure, increasing the likelihood that parasites successfully colonise new hosts and expand their niche (Mestre, Poulin & Hortal, 2020). For example, multiple lineages of vector-borne haemosporidians infecting migratory birds have independently evolved year-round transmission, seemingly by adopting a wide range of blood-feeding insects that may act as suitable vectors in both their host's breeding and wintering grounds (Pérez-Tris & Bensch, 2005).…”

Disturbance‐induced emigration: an overlooked mechanism that reduces metapopulation extinction risk

“…However, the metapopulation concept has been extended to describe dynamics of organisms that inhabit ephemeral habitats, in which habitat life span is similar to or shorter than population life span (Reigada et al 2015). For instance, dynamics of horizontally transmitted symbionts may fit this metapopulation archetype if hosts are conceptualized as ephemeral patches (Mestre et al 2020). Host death can be viewed as a patch disturbance for its resident symbionts.…”

“…Because hosts are born and die, they are ephemeral patches with a finite lifetime, so recurrent colonization of fresh hosts is required for symbiont persistence in a host population. Many symbionts disperse via horizontal transmission from one host to another, and such systems are strongly akin to classical metapopulations, in that host death is in effect a severe patch disturbance for its resident symbionts (Mestre et al 2020). But host death is not always a dead end for symbionts (Ponton et al 2006, Klose et al 2012, Rizvi et al 2012.…”