Host–pathogen coevolution, secondary sympatry and species diversification

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125

The rate at which speciation occurs varies greatly among different kinds of organisms and is frequently assumed to result from species-or clade-specific factors that influence the rate at which populations acquire reproductive isolation. This premise leads to a fundamental prediction that has never been tested: Organisms that quickly evolve prezygotic or postzygotic reproductive isolation should have faster rates of speciation than organisms that slowly acquire reproductive isolation. We combined phylogenetic estimates of speciation rates from Drosophila and birds with a method for analyzing interspecific hybridization data to test whether the rate at which individual lineages evolve reproductive isolation predicts their macroevolutionary rate of species formation. We find that some lineages evolve reproductive isolation much more quickly than others, but this variation is decoupled from rates of speciation as measured on phylogenetic trees. For the clades examined here, reproductive isolation-especially intrinsic, postzygotic isolation-does not seem to be the rate-limiting control on macroevolutionary diversification dynamics. These results suggest that factors associated with intrinsic reproductive isolation may have less to do with the tremendous variation in species diversity across the evolutionary tree of life than is generally assumed. A central challenge at the interface between macroevolution and microevolution is to explain the population-level processes that contribute to biological variation in diversification rates and species richness (1). Phylogenetic evidence for biological variation in the rate of species diversification is widespread (2, 3), and numerous studies have now linked specific traits to the dynamics of speciation and extinction as realized over macroevolutionary timescales (2,4). At the population level, a microevolutionary research program on the biology of speciation has focused on the factors that lead to various forms of reproductive isolation (RI) between populations (5, 6). Explaining how and why RI evolves is generally considered to be the central and defining challenge in the study of speciation (2, 7-9), and recent studies have made great progress toward explaining the genetic and ecological basis for various forms of RI (7,8,10).Most microevolutionary research on speciation implicitly assumes that RI is the defining and rate-limiting step in the speciation process (7,8,11), but the evolution of RI need not bear any predictive relationship to rates of species diversification as realized over macroevolutionary timescales (12). This has long been recognized by the paleontological community, where "successful" speciation is believed to entail not only the evolution of reproductive isolation but also the persistence of incipient species (13-15). For example, speciation might be limited primarily by the rate at which lineages form allopatric isolates (6,16) or by the capacity for geographic range expansion (17, 18). Likewise, speciation might be limited more by factors that influe...

Section: Groupmentioning

confidence: 99%

Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds

Rabosky

Matute

2013

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125

“…Suppression of pathogens leading to high population productivity, saturation of niche space, and broad geographic distribution might increase opportunities for population subdivision and species formation. I have argued elsewhere that specialized pathogens might prevent secondary sympatry by sister taxa and reduce diversification within clades (105,106). Suppression of pathogens would reduce this impediment to diversification.…”

Section: )mentioning

confidence: 99%

Evolutionary diversification, coevolution between populations and their antagonists, and the filling of niche space

Ricklefs

2010

Self Cite

212

218

The population component of a species' niche corresponds to the distribution of individuals across environments within a region. As evolutionary clades of species diversify, they presumably fill niche space, and, consequently, the rate of increase in species numbers slows. Total niche space and species numbers appear to be relatively stable over long periods, and so an increase in the species richness of one clade must be balanced by decrease in others. However, in several analyses, the total population niche space occupied per clade is independent of the number of species, suggesting that species in more diverse clades overlap more in niche space. This overlap appears to be accommodated by variation in the populations of each species, including their absence, within suitable niche space. I suggest that the uneven filling of niche space results from localized outcomes of the dynamic coevolutionary interactions of populations with their pathogens or other antagonists. Furthermore, I speculate that relationships with pathogens might constrain diversification if pathogen diversity increased with host diversity and resulted in more frequent host switching and emergent disease. Many indirect observations are consistent with these scenarios. However, the postulated influence of pathogens on the filling of niche space and diversification of clades primarily highlights our lack of knowledge concerning the space and time dimensions of coevolutionary interactions and their influence on population distribution and species diversification. mosaic evolution | niche breadth | pathogen E ach species occupies a part of the ecological space available in the environment, usually referred to as its "ecological niche." Although the niche has been difficult to define precisely, most treatments consider conditions of the physical environment, characteristics of resources-whether soil nutrients, plants, or animal prey-and the traits of other interacting species (i.e., competitors, mutualists, predators, and pathogens) as important axes of ecological space that are partitioned among species (1, 2). In this essay, I distinguish individual and population niche space, the former reflecting primarily evolutionary adaptations of individuals to exploit resources and the latter, primarily reflecting demographic processes maintaining populations at a particular place. Of course, the population component of the niche also is influenced by adaptations of individuals to the range of environmental conditions over space within a region.Both components of niche space can be defined for any particular species and also for a set of species, of which those comprising an evolutionary clade descended from a common ancestor are most relevant here. Adaptive radiations of species fill niche space by evolutionary diversification, yet both phylogenetic analyses (3, 4) and paleontological studies (5, 6) suggest that diversification is constrained and that individual clades typically enjoy a limited period of rapid radiation early in their existence. The number...

“…Specialized associations between specific parasites and vectors (20-22) may drive such heterogeneity, although a recent analysis suggests that parasitehost compatibility is also important (23), and local coevolutionary relationships between parasites and their hosts likely influence geographic distributions of both host and parasite populations (11,14,15). However, most regional studies of these parasites have focused on individual host species (24-30).…”

mentioning

confidence: 99%

Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites

Ellis

Collins

Medeiros

et al. 2015

Self Cite

The drivers of regional parasite distributions are poorly understood, especially in comparison with those of free-living species. For vector-transmitted parasites, in particular, distributions might be influenced by host-switching and by parasite dispersal with primary hosts and vectors. We surveyed haemosporidian blood parasites (Plasmodium and Haemoproteus) of small land birds in eastern North America to characterize a regional parasite community. Distributions of parasite populations generally reflected distributions of their hosts across the region. However, when the interdependence between hosts and parasites was controlled statistically, local host assemblages were related to regional climatic gradients, but parasite assemblages were not. Moreover, because parasite assemblage similarity does not decrease with distance when controlling for host assemblages and climate, parasites evidently disperse readily within the distributions of their hosts. The degree of specialization on hosts varied in some parasite lineages over short periods and small geographic distances independently of the diversity of available hosts and potentially competing parasite lineages. Nonrandom spatial turnover was apparent in parasite lineages infecting one host species that was well-sampled within a single year across its range, plausibly reflecting localized adaptations of hosts and parasites. Overall, populations of avian hosts generally determine the geographic distributions of haemosporidian parasites. However, parasites are not dispersal-limited within their host distributions, and they may switch hosts readily.avian malaria | community assembly | emerging infectious disease | Haemosporida | parasite communities A regional community can be thought of as a set of species whose distributions partially overlap within a large geographic area (1, 2). The structure of the regional community (i.e., the relative abundances of species across space and the degree to which populations cooccur) is governed by local (e.g., interspecific competition) and regional (e.g., species diversification and dispersal) processes (3). Although regional communities include all species, parasites and pathogens are rarely considered integral community members (4). Indeed, impacts of parasites on community structure are frequently associated with epidemicsoften following introductions to nonnative regions-that have driven naïve hosts to extinction or near extinction (5-7). However, parasites likely play a critical role in shaping regional community structure. Parasites can comprise a large proportion of the community biomass (8), form the majority of links in a community food web (9), and influence regional diversity by variously accelerating (10) or slowing (11) host diversification.Nevertheless, few studies have investigated the processes influencing the regional community structure of both parasites and their hosts. Parasite populations are integrated into community studies with difficulty, partly because these populations are distributed across multiple...