Range Expansion Drives Dispersal Evolution In An Equatorial Three-Species Symbiosis

A-09-14International audienceBackground Recurrent climatic oscillations have produced dramatic changes in species distributions. This process has been proposed to be a major evolutionary force, shaping many life history traits of species, and to govern global patterns of biodiversity at different scales. During range expansions selection may favor the evolution of higher dispersal, and symbiotic interactions may be affected. It has been argued that a weakness of climate fluctuation-driven range dynamics at equatorial latitudes has facilitated the persistence there of more specialized species and interactions. However, how much the biology and ecology of species is changed by range dynamics has seldom been investigated, particularly in equatorial regions. Methodology/Principal Findings We studied a three-species symbiosis endemic to coastal equatorial rainforests in Cameroon, where the impact of range dynamics is supposed to be limited, comprised of two species-specific obligate mutualists –an ant-plant and its protective ant– and a species-specific ant parasite of this mutualism. We combined analyses of within-species genetic diversity and of phenotypic variation in a transect at the southern range limit of this ant-plant system. All three species present congruent genetic signatures of recent gradual southward expansion, a result compatible with available regional paleoclimatic data. As predicted, this expansion has been accompanied by the evolution of more dispersive traits in the two ant species. In contrast, we detected no evidence of change in lifetime reproductive strategy in the tree, nor in its investment in food resources provided to its symbiotic ants. Conclusions/Significance Despite the decreasing investment in protective workers and the increasing investment in dispersing females by both the mutualistic and the parasitic ant species, there was no evidence of destabilization of the symbiosis at the colonization front. To our knowledge, we provide here the first evidence at equatorial latitudes that biological traits associated with dispersal are affected by the range expansion dynamics of a set of interacting species

Dynamics of species coexistence : maintenance of a plant-ant competitive metacommunity

The metacommunity approach is an adequate framework to study coexistence between interacting species at different spatial scales. However, empirical evidence from natural metacommunities necessary to evaluate the predictive power of theoretical models of species coexistence remains sparse. We use two African ant species, Cataulacus mckeyi and Petalomyrmex phylax, symbiotically associated with the myrmecophyte Leonardoxa africana africana, to examine spatio-temporal dynamics of species coexistence and to investigate which environmental and life-history parameters may contribute to the maintenance of species diversity in this guild of symbiotic ants. Using environmental niche partitioning as a conceptual framework, we combined data on habitat variation, social structure of colonies, and population genetics with data from a colonisation experiment and from observation of temporal dynamics. We propose that the dynamics of ant species colonisation and replacement at local and regional scales can be explained by a set of life history traits for which the two ants exhibit hierarchies, coupled with strong environmental differences between the different patches in the level of environmental disturbances. The role of the competition-colonisation tradeoff is discussed and we propose that interspecific tradeoffs for traits related to dispersal and to reproduction are also determinant for species coexistence. We therefore suggest that species-sorting mechanisms are predominant in the dynamics of this metacommunity, but we also emphasise that there may be many ways for two symbionts in competition for the same host to coexist. The results speak in favour of a more complete integration of the various metacommunity models in a single theoretical framework. © 2009 Oikos.SCOPUS: ar.jFLWINinfo:eu-repo/semantics/publishe

Changes in mating system and social structure of the ant Petalomyrmex phylax are associated with range expansion in Cameroon

Correspondance: [email protected] audiencePast climate shifts have led to major oscillations in species distributions. Hence historical contingencies and selective processes occurring during such phases may be determinants for understanding the forces that have shaped extant phenotypes. In the plant-ant Petalomyrmex phylax (Formicinae), we observed spatial variation in number of queens in mature colonies, from several queens (high polygyny) in the median part of its distribution to a moderate number of queens (weak polygyny) or even only a single queen (monogyny) in the southwestern most populations. This variation did not correlate with indicators of variation in current nest site availability and colony turnover, the supposedly determinant selective forces acting on gyny in ants. We show here that the variation in social structure correlates with a historical process corresponding to a progressive colonization of coastal southern Cameroon by the ant. Using microsatellite markers, we observed a clear pattern of isolation by distance except for the southernmost populations. Measures of genetic variability that do not take into account allele size were at equilibrium in all except the southernmost populations, suggesting recent foundation of the latter. Measures of genetic diversity taking into account allele size showed a clinal north-south decrease in variance of allele size. We propose that southern populations have yet to regain allele size variance after bottlenecks associated with the foundation of new populations, and that this variance is regained over time. Hence variation in social structure mirrors an old but still active southward colonization process or metapopulation dynamics, possibly in association with an expansion of the rain forest habitat during the late Holocene. A low number of queens in ant colonies is typically associated with strong dispersal capacity. We therefore suggest that the initial founders of new populations belong to the monogynous to weakly polygynous phenotype, and that queen number progressively increases in older population

Integrative taxonomy of a poorly known Sahelian rodent, Gerbillus nancillus (Muridae, Gerbillinae)

Aridification processes that affected the Sahelian area of West Africa during the last decades have induced significant changes in plant and animal communities of this region. In rodents, the genus Gerbillus characteristic of North African and Asian arid habitats has been affected by this climatic and environmental trends. Several species of this genus showed a southward range expansion in recent years into the Sahelian bioclimatic zone. Recent sampling in several localities of West Africa (Mali, Niger and Senegal) enabled us to collect numerous specimens of small gerbils. An integrative study of these samples using molecular, morphological and cytogenetical methods revealed that many of them were attributable to Gerbillus nancillus, a secretive and poorly known species. Gerbillus nancillus appears characterized by a well differentiated karyotype with 2n = 56 chromosomes, and to represent a unique genetic lineage within this genus. Body and skull measurements of G. nancillus were compared with those of the morphologically similar Gerbillus henleyi, which provided diagnostic clues between them. These new data significantly expand the distribution area of G. nancillus, which now ranges from Sudan in the East to Senegal in the West. G. nancillus is here reported from numerous new localities in Niger and Mali, and for the first time in Senegal, which raises questions about the origin of its presence and the colonization routes it followed to get there. We also show that G. henleyi and G. nancillus are sympatric and apparently often syntopic in the sub-Saharan part of the distribution of G. henleyi

Leishmania major and Trypanosoma lewisi infection in invasive and native rodents in Senegal.

Bioinvasion is a major public health issue because it can lead to the introduction of pathogens in new areas and favours the emergence of zoonotic diseases. Rodents are prominent invasive species, and act as reservoirs in many zoonotic infectious diseases. The aim of this study was to determine the link between the distribution and spread of two parasite taxa (Leishmania spp. and Trypanosoma lewisi) and the progressive invasion of Senegal by two commensal rodent species (the house mouse Mus musculus domesticus and the black rat Rattus rattus). M. m. domesticus and R. rattus have invaded the northern part and the central/southern part of the country, respectively. Native and invasive rodents were caught in villages and cities along the invasion gradients of both invaders, from coastal localities towards the interior of the land. Molecular diagnosis of the two trypanosomatid infections was performed using spleen specimens. In the north, neither M. m. domesticus nor the native species were carriers of these parasites. Conversely, in the south, 17.5% of R. rattus were infected by L. major and 27.8% by T. lewisi, while very few commensal native rodents were carriers. Prevalence pattern along invasion gradients, together with the knowledge on the geographical distribution of the parasites, suggested that the presence of the two parasites in R. rattus in Senegal is of different origins. Indeed, the invader R. rattus could have been locally infected by the native parasite L. major. Conversely, it could have introduced the exotic parasite T. lewisi in Senegal, the latter appearing to be poorly transmitted to native rodents. Altogether, these data show that R. rattus is a carrier of both parasites and could be responsible for the emergence of new foci of cutaneous leishmaniasis, or for the transmission of atypical human trypanosomiasis in Senegal

Range expansion of the invasive house mouse Mus musculus domesticus in Senegal, West Africa : a synthesis of trapping data over three decades, 1983-2014

The worldwide intensification of human-associated exchanges favours the multiplication of biological invasions. Among mammals, rodent species, including the house mouse Mus musculus, are identified as major invaders with profound impacts on native biodiversity, human health and activities. Though contemporary rodent invasions are described on several islands, there are few data describing ongoing house mouse invasions in continental areas. We first outline the known picture of the distribution of the house mouse in Africa. We then describe the ongoing range expansion of the house mouse in Senegal, in order to update its distribution area, assess the location of the invasion front, describe the spatio-temporal dynamics of the invasion at the country scale and evaluate its impact on native small mammal communities. We briefly review the worldwide status of the house mouse, with special focus on its situation in Africa. Focusing on Senegal, we then use historical records and a large body of spatio-temporal indoor trapping data obtained from small mammal communities over the last 30 years to analyse the invasion dynamics of the subspecies at the scale of the country. The geographic range of the invasive house mouse is surprisingly poorly known in Africa. In Senegal, we document a large range expansion of the subspecies in human settlements over the whole country within the last 30 years. The invasion is still ongoing further east and south within the country, and has major consequences for small mammal communities and thus probably for risks associated with zoonotic diseases

Contemporary evolution of immunity during range expansion of two invasive rodents in Senegal

Biological invasions provide unique opportunities for studying life history trait changes over contemporary time scales. As spatial spread may be related to changes in parasite communities, several hypotheses (such as the evolution of increased competitive ability (EICA) or EICA-refined hypotheses) suggest immune changes in invasive species along invasion gradients. Although native hosts may be subject to similar changes in parasite selection pressures, their immune responses have been rarely investigated in invasion contexts. In this study, we evaluated immune variations for invasive house mice Mus musculus domesticus, invasive black rats Rattus rattus and native rodents Mastomys erythroleucus and Mastomys natalensis along well-characterised invasion gradients in Senegal. We focused on antibody-mediated (natural antibodies and complement) and inflammatory (haptoglobin) responses. One invasion route was considered for each invasive species, and environmental conditions were recorded. Natural-antibody mediated responses increased between sites of long-established invasion and recently invaded sites only in house mice. Both invasive species exhibited higher inflammatory responses at the invasion front than in sites of long-established invasion. The immune responses of native species did not change with the presence of invasive species. These patterns of immune variations do not support the EICA and EICA refined hypotheses, and they rather suggest a higher risk of exposure to parasites on the invasion front. Altogether, these results provide a first basis to further assess the role of immune changes in invasion success

Contemporary variations of immune responsiveness during range expansion of two invasive rodents in Senegal

Biological invasions provide unique opportunities for studying life history trait changes over contemporary time scales. As spatial spread may be related to changes in parasite communities, several hypotheses (such as the evolution of increased competitive ability (EICA) or EICA-refined hypotheses) suggest immune changes in invasive species along invasion gradients. Although native hosts may be subject to similar changes in parasite selection pressures, their immune responses have been rarely investigated in invasion contexts. In this study, we evaluated immune variations for invasive house mice Mus musculus domesticus, invasive black rats Rattus rattus and native rodents Mastomys erythroleucus and Mastomys natalensis along well-characterised invasion gradients in Senegal. We focused on antibody-mediated (natural antibodies and complement) and inflammatory (haptoglobin) responses. One invasion route was considered for each invasive species, and environmental conditions were recorded. Natural-antibody mediated responses increased between sites of long-established invasion and recently invaded sites only in house mice. Both invasive species exhibited higher inflammatory responses at the invasion front than in sites of long-established invasion. The immune responses of native species did not change with the presence of invasive species. These patterns of immune variations do not support the EICA and EICA refined hypotheses, and they rather suggest a higher risk of exposure to parasites on the invasion front. Altogether, these results provide a first basis to further assess the role of immune changes in invasion success

Maritime international trade and bioinvasions: A three‐year long survey of small mammals in Autonomous Port of Cotonou, Benin

International audience1. International trade has been favouring the dissemination of a wide suite of invasive alien species. Upstream prevention through the monitoring of entry points is identified as an appropriate strategy to achieve control of bioinvasions and their consequences. Maritime transportation has been responsible for the introduction worldwide of exotic rodents that are major pests for crops and food stocks as well as reservoirs of many zoonotic pathogens. In order to limit further dissemination, the International Health Regulation constrains decisions makers and socio-economic stakeholders to manage ship-mediated import/export of rodents within seaports.2. Unfortunately, eco-evolutionary insights into rodent introduction events that could guide preventive actions in seaports are very scarce. In order to bridge this gap, we here describe the results of a 3 year-long survey of small mammals conducted in the Port of Cotonou, Benin.3. Our aim was to assess the spatiotemporal distribution, diversity and relative abundance of invasive and native rodents.4. 960 small mammal individuals were captured in nine within-seaport sites. We found (i) a marked predominance of invasive species (84% of the individuals belonging to Mus musculus, Rattus rattus, R. norvegicus), (ii) with native species (i.e. Mastomys natalensis and the shrew Crocidura olivieri) essentially restricted to peripheral non-industrial areas, as well as (iii) a fine-scale spatial segregation stable over time between the invasive Norway rats and house mice on the one hand, and the black rats and shrews on the other hand.5. Furthermore, trapping before and after two successive rodent control campaigns indicates that they were ineffective and that subsequent rodent recolonisation occurred 6–12 months following intervention.6. Synthesis and applications. Our results are discussed in terms of ecological processes at play (e.g. interspecific interactions) and operational recommendations (e.g. assessment of proper eradication units, environmental modifications)

Sharing space between native and invasive small mammals: Study of commensal communities in Senegal

International audienceUrbanization processes are taking place at a very high rate, especially in Africa. At the same time, a number of small mammal species, be they native or invasive, take advantage of human-induced habitat modifications. They represent commensal communities of organisms that cause a number of inconveniences to humans, including potential reservoirs of zoonotic diseases. We studied via live trapping and habitat characterization such commensal small mammal communities in small villages to large cities of Senegal, to try to understand how the species share this particular space. Seven major species were recorded, with exotic invasive house mice (Mus musculus) and black rats (Rattus rattus) dominating in numbers. The shrew Crocidura olivieri appeared as the main and more widespread native species, while native rodent species (Mastomys natalensis, M. erythroleucus, Arvicanthis niloticus and Praomys daltoni) were less abundant and/or more localized. Habitat preferences, compared between species in terms of room types and characteristics, showed differences among house mice, black rats and M. natalensis especially. Niche (habitat component) breadth and overlap were measured. Among invasive species, the house mouse showed a larger niche breadth than the black rat, and overall, all species displayed high overlap values. Co-occurrence patterns were studied at the global and local scales. The latter show cases of aggregation (between the black rat and native species, for instance) and of segregation (as between the house mouse and the black rat in Tambacounda, or between the black rat and M. natalensis in Kédougou). While updating information on commensal small mammal distribution in Senegal, a country submitted to a dynamic process of invasion by the black rat and the house mouse, we bring original information on how species occupy and share the commensal space, and make predictions on the evolution of these communities in a period of ever-accelerating global changes