Dispersal is a major driver of the latitudinal diversity gradient of Carnivora

AimUnderstanding the relative contribution of diversification rates (speciation and extinction) and dispersal in the formation of the latitudinal diversity gradient - the decrease in species richness with increasing latitude - is a main goal of biogeography. The mammalian order Carnivora, which comprises 286 species, displays the traditional latitudinal diversity gradient seen in almost all mammalian orders. Yet the processes driving high species richness in the tropics may be fundamentally different in this group from that in other mammalian groups. Indeed, a recent study suggested that in Carnivora, unlike in all other major mammalian orders, net diversification rates are not higher in the tropics than in temperate regions. Our goal was thus to understand the reasons why there are more species of Carnivora in the tropics. LocationWorld-wide. MethodsWe reconstructed the biogeographical history of Carnivora using a time-calibrated phylogeny of the clade comprising all terrestrial species and dispersal-extinction-cladogenesis models. We also analysed a fossil dataset of carnivoran genera to examine how the latitudinal distribution of Carnivora varied through time. ResultsOur biogeographical analyses suggest that Carnivora originated in the East Palaearctic (i.e. Central Asia, China) in the early Palaeogene. Multiple independent lineages dispersed to low latitudes following three main paths: toward Africa, toward India/Southeast Asia and toward South America via the Bering Strait. These dispersal events were probably associated with local extinctions at high latitudes. Fossil data corroborate a high-latitude origin of the group, followed by late dispersal events toward lower latitudes in the Neogene. Main conclusionsUnlike most other mammalian orders, which originated and diversified at low latitudes and dispersed out of the tropics', Carnivora originated at high latitudes, and subsequently dispersed southward. Our study provides an example of combining phylogenetic and fossil data to understand the generation and maintenance of global-scale geographical variations in species richness.

How differential management strategies affect Ips typographus L. dispersal

Bark beetle outbreaks have a devastating effect on economically important forests worldwide, thus requiring extensive application of management control strategies. The presence of unmanaged protected areas in close proximity to managed forests can instigate concerns that bark beetle infestations may spread from unmanaged into managed stands. We studied the impact of differential management of forest stands on the dispersal dynamics of the European spruce bark beetle, Ips typographus, making use of inferential population genetics on mitochondrial and nuclear genomes. Bayesian inferences of migration rates and a most parsimonious dispersal tree show that outgoing gene flow was consistently higher from managed to unmanaged areas. Reason for that is likely the thorough removal of potential breeding material in managed forests and thus the dispersal of the base stock beetles from these areas to unmanaged areas where breeding material is available. Our study suggests that the potential threat posed by unmanaged to managed forests in regard to I. typographus infestation needs to be carefully re-considered.

Pre-dispersal predation effect on seed packaging strategies and seed viability.

An increased understanding of intraspecific seed packaging (i.e. seed size/number strategy) variation across different environments may improve current knowledge of the ecological forces that drive seed evolution in plants. In particular, pre-dispersal seed predation may influence seed packaging strategies, triggering a reduction of the resources allocated to undamaged seeds within the preyed fruits. Assessing plant reactions to pre-dispersal seed predation is crucial to a better understanding of predation effects, but the response of plants to arthropod attacks remains unexplored. We have assessed the effect of cone predation on the size and viability of undamaged seeds in populations of Juniperus thurifera with contrasting seed packaging strategies, namely, North African populations with single-large-seeded cones and South European populations with multi-small-seeded cones. Our results show that the incidence of predation was lower on the single-large-seeded African cones than on the multi-small-seeded European ones. Seeds from non-preyed cones were also larger and had a higher germination success than uneaten seeds from preyed cones, but only in populations with multi-seeded cones and in cones attacked by Trisetacus sp., suggesting a differential plastic response to predation. It is possible that pre-dispersal seed predation has been a strong selective pressure in European populations with high cone predation rates, being a process which maintains multi-small-seeded cones and empty seeds as a strategy to save some seeds from predation. Conversely, pre-dispersal predation might not have a strong effect in the African populations with single-large-seeded cones characterized by seed germination and filling rates higher than those in the European populations. Our results indicate that differences in pre-dispersal seed predators and predation levels may affect both selection on and intraspecific variation in seed packaging.

Social chromosome variants differentially affect queen determination and the survival of workers in the fire ant Solenopsis invicta.

Intraspecific variation in social organization is common, yet the underlying causes are rarely known. An exception is the fire ant Solenopsis invicta in which the existence of two distinct forms of social colony organization is under the control of the two variants of a pair of social chromosomes, SB and Sb. Colonies containing exclusively SB/SB workers accept only one single queen and she must be SB/SB. By contrast, when colonies contain more than 10% of SB/Sb workers, they accept several queens but only SB/Sb queens. The variants of the social chromosome are associated with several additional important phenotypic differences, including the size, fecundity and dispersal strategies of queens, aggressiveness of workers, and sperm count in males. However, little is known about whether social chromosome variants affect fitness in other life stages. Here, we perform experiments to determine whether differential selection occurs during development and in adult workers. We find evidence that the Sb variant of the social chromosome increases the likelihood of female brood to develop into queens and that adult SB/Sb workers, the workers that cull SB/SB queens, are overrepresented in comparison to SB/SB workers. This demonstrates that supergenes such as the social chromosome can have complex effects on phenotypes at various stages of development.

Population demography and the evolution of helping behaviors.

Limited dispersal may favor the evolution of helping behaviors between relatives as it increases their relatedness, and it may inhibit such evolution as it increases local competition between these relatives. Here, we explore one way out of this dilemma: if the helping behavior allows groups to expand in size, then the kin-competition pressure opposing its evolution can be greatly reduced. We explore the effects of two kinds of stochasticity allowing for such deme expansion. First, we study the evolution of helping under environmental stochasticity that may induce complete patch extinction. Helping evolves if it results in a decrease in the probability of extinction or if it enhances the rate of patch recolonization through propagules formed by fission of nonextinct groups. This mode of dispersal is indeed commonly found in social species. Second, we consider the evolution of helping in the presence of demographic stochasticity. When fecundity is below its value maximizing deme size (undersaturation), helping evolves, but under stringent conditions unless positive density dependence (Allee effect) interferes with demographic stochasticity. When fecundity is above its value maximizing deme size (oversaturation), helping may also evolve, but only if it reduces negative density-dependent competition.

Proximity-dependent pollen performance in Silene vulgaris.

BACKGROUND AND AIMS: Pollen and seed dispersal in herbaceous insect-pollinated plants are often restricted, inducing strong population structure. To what extent this influences mating within and among patches is poorly understood. This study investigates the influence of population structure on pollen performance using controlled pollinations and genetic markers. METHODS: Population structure was investigated in a patchily distributed population of gynodioecious Silene vulgaris in Switzerland using polymorphic microsatellite markers. Experimental pollinations were performed on 21 hermaphrodite recipients using pollen donors at three spatial scales: (a) self-pollination; (b) within-patch cross-pollinations; and (c) between-patch cross-pollinations. Pollen performance was then compared with respect to crossing distance. KEY RESULTS: The population of S. vulgaris was characterized by a high degree of genetic sub-structure, with neighbouring plants more related to one another than to distant individuals. Inbreeding probably results from both selfing and biparental inbreeding. Pollen performance increased with distance between mates. Between-patch pollen performed significantly better than both self- and within-patch pollen donors. However, no significant difference was detected between self- and within-patch pollen donors. CONCLUSIONS: The results suggest that population structure in animal-pollinated plants is likely to influence mating patterns by favouring cross-pollinations between unrelated plants. However, the extent to which this mechanism could be effective as a pre-zygotic barrier preventing inbred mating depends on the patterns of pollinator foraging and their influence on pollen dispersal.

Discordances between phylogenetic and morphological patterns in alpine leaf beetles attest to an intricate biogeographic history of lineages in postglacial Europe.

Pleistocene glacial and interglacial periods have moulded the evolutionary history of European cold-adapted organisms. The role of the different mountain massifs has, however, not been accurately investigated in the case of high-altitude insect species. Here, we focus on three closely related species of non-flying leaf beetles of the genus Oreina (Coleoptera, Chrysomelidae), which are often found in sympatry within the mountain ranges of Europe. After showing that the species concept as currently applied does not match barcoding results, we show, based on more than 700 sequences from one nuclear and three mitochondrial genes, the role of biogeography in shaping the phylogenetic hypothesis. Dating the phylogeny using an insect molecular clock, we show that the earliest lineages diverged more than 1 Mya and that the main shift in diversification rate occurred between 0.36 and 0.18 Mya. By using a probabilistic approach on the parsimony-based dispersal/vicariance framework (MP-DIVA) as well as a direct likelihood method of state change optimization, we show that the Alps acted as a cross-roads with multiple events of dispersal to and reinvasion from neighbouring mountains. However, the relative importance of vicariance vs. dispersal events on the process of rapid diversification remains difficult to evaluate because of a bias towards overestimation of vicariance in the DIVA algorithm. Parallels are drawn with recent studies of cold-adapted species, although our study reveals novel patterns in diversity and genetic links between European mountains, and highlights the importance of neglected regions, such as the Jura and the Balkanic range.

Phylogeographical footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew, Crocidura russula (Mammalia: Soricidae).

We used mitochondrial cyt b sequences to investigate the phylogenetic relationships of Crocidura russula (sensu lato) populations across the Strait of Gibraltar, western Europe, Maghreb, and the Mediterranean and Atlantic islands. This revealed very low genetic divergence between European and Moroccan populations. The application of a molecular clock previously calibrated for shrews suggested that the separation of European from Moroccan lineages occurred less than 60 000 bp, which is at least 5 million years (Myr) after the reopening of the Strait of Gibraltar. This means that an overwater dispersal event was responsible for the observed phylogeographical structure. In contrast, genetic analyses revealed that Moroccan populations were highly distinct from Tunisian ones. According to the molecular clock, these populations separated about 2.2 million years ago (Ma), a time marked by sharp alternations of dry and humid climates in the Maghreb. The populations of the Mediterranean islands Ibiza, Pantelleria, and Sardinia were founded from Tunisian populations by overwater dispersal. In conclusion, overwater dispersal across the Strait of Gibraltar, probably assisted by humans, is possible for small terrestrial vertebrates. Moreover, as in Europe, Quaternary climatic fluctuations had a major effect on the phylogeographical structure of the Maghreb biota.

Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration.

Local adaptation is a major mechanism underlying the maintenance of phenotypic variation in spatially heterogeneous environments. In the barn owl (Tyto alba), dark and pale reddish-pheomelanic individuals are adapted to conditions prevailing in northern and southern Europe, respectively. Using a long-term dataset from Central Europe, we report results consistent with the hypothesis that the different pheomelanic phenotypes are adapted to specific local conditions in females, but not in males. Compared to whitish females, reddish females bred in sites surrounded by more arable fields and less forests. Colour-dependent habitat choice was apparently beneficial. First, whitish females produced more fledglings when breeding in wooded areas, whereas reddish females when breeding in sites with more arable fields. Second, cross-fostering experiments showed that female nestlings grew wings more rapidly when both their foster and biological mothers were of similar colour. The latter result suggests that mothers should particularly produce daughters in environments that best match their own coloration. Accordingly, whiter females produced fewer daughters in territories with more arable fields. In conclusion, females displaying alternative melanic phenotypes bred in habitats providing them with the highest fitness benefits. Although small in magnitude, matching habitat selection and local adaptation may help maintain variation in pheomelanin coloration in the barn owl.

Secondary contact zones and hybridizations: the case of the lesser white-toothed shrew (Crocidura suaveolens group, Soricidae)

In the present study, we analyzed 58 samples of the lesser white-toothed shrew group (Crocidura suaveolens) from eastern Europe and Turkey, where, according to previous publications, three different mitochondrial and nuclear lineages are present. We sequenced 799 bp of the nuclear BRCA1 gene and 400 bp of the mitochondrial cytochrome b gene to: (1) determine a potential contact zone between the lineages; (2) detect hybridizations and introgressions between them; and (3) comment on the level of reproductive isolation of the different lineages. We revealed two zones of hybridization in Turkey, of which the first occurred west of the Bosphorus Straits (three hybrids) and the second in Anatolia (twelve hybrids). In the latter, the nuclear markers revealed a large zone of hybridization, of approximately 600 km. It also revealed that hybrids of first, second, and later generations are present within the populations, and therefore that the reproductive isolation between the different lineages is weak.

Le nombre de reines chez les fourmis et sa conséquence sur l'organisations sociale

Nearly half of all ant species form polygyne societies (cohabitation of more than a single egg-laying queen). These queens are generally smaller and store fewer fat reserves than queens from monogyne colonies. Most queens in polygyne colonies (70-100 pour 100) are inseminated, although this proportion varies among species, and even among populations of the same species. They exhibit mutual tolerance and they all contribute to the reproductive effort of the colony. Nevertheless, their individual fecundity is considerably reduced compared with that of queens from monogyne colonies. This reduction in fecundity seems to be due to some form of mutual inhibition, in some cases the secretion by each female of a substance suppressing egg production in other queens has been implicated. In a few species, queens are organized into a hierarchy such that certain queens lay more eggs than others or even monopolize egg-laying (functional monogyny). Polygyny is linked to a particular life history. It rarely results from the association of several foundresses (primary polygyny). Usually, it is due to the adoption of young queens by an established nest just after a nuptial flight. This secondary polygyny means that the dispersal of the species is limited and is achieved by the budding of a mother nest. Thus colony founding is dependent; with workers accompanying young queens in establishing new colonies. Observation of closely related species exhibiting different social organizations, some monogyne and others polygyne, shows a possible link between queen number and ecological conditions: polygyne forms are more frequent in unstable habitats susceptible to rapid change, such as that caused by human activity. The existence of polygyne societies is an intriguing evolutionary mystery. Research into the origin and maintenance of polygyny focuses on patterns of speciation in relation to queen number and the different theories put forth for the evolution of eusociality, mainly kin selection and mutualism.

The evolution of inbred social systems in spiders and other organisms: from short-term gains to long-term evolutionary dead-ends?

The question of why some social systems have evolved close inbreeding is particularly intriguing given expected short- and long-term negative effects of this breeding system. Using social spiders as a case study, we quantitatively show that the potential costs of avoiding inbreeding through dispersal and solitary living could have outweighed the costs of inbreeding depression in the origin of inbred spider sociality. We further review the evidence that despite being favored in the short term, inbred spider sociality may constitute in the long run an evolutionary dead end. We also review other cases, such as the naked mole rats and some bark and ambrosia beetles, mites, psocids, thrips, parasitic ants, and termites, in which inbreeding and sociality are associated and the evidence for and against this breeding system being, in general, an evolutionary dead end.

Stay or drift? Queen acceptance in the ant Formica paralugubris

The acceptance of new queens in ant colonies has profound effects on colony kin structure and inclusive fitness of workers. Therefore, it is important to study the recognition and discrimination behaviour of workers towards reproductive individuals entering established colonies. We examined the acceptance rate of queens in populations of the highly polygynous ant F. paralugubris, where the genetic differentiation among nests and discrimination ability among workers suggest that workers might reject foreign queens. We experimentally introduced young queens in their natal nest and in foreign nests. Surprisingly, the survival rate of mated queens did not differ significantly when introduced in a foreign male-producing nest, a foreign female-producing nest, or the natal nest. Moreover, the survival of virgin queens in their natal nest was twice the one of mated queens, suggesting that mating status plays an important role for acceptance. The results indicate that other factors than queen discrimination by workers are implicated in the limited long-distance gene flow between nests in these populations.

Mass effects mediate coexistence in competing shrews.

Recent developments in metacommunity theory have raised awareness that processes occurring at regional scales might interfere with local dynamics and affect conditions for the local coexistence of competing species. Four main paradigms are recognized in this context (namely, neutral, patch-dynamics, species-sorting, and mass-effect), which differ according to the role assigned to ecological or life-history differences among competing species, as well as to the relative time scale of regional vs. local dynamics. We investigated the patterns of regional and local coexistence of two species of shrews (Crocidura russula and Sorex coronatus) sharing a similar diet (generalist insectivores) over four generations, in a spatially structured habitat at the altitudinal limit of their distributions. Local populations were small, and regional dynamics were strong, with high rates of extinction and recolonization. Niche analysis revealed significant habitat differentiation on a few important variables, including temperature and availability of winter resting sites. In sites suitable for both species, we found instances of local coexistence with no evidence of competitive exclusion. Patterns of temporal succession did not differ from random, with no suggestion of a colonization-competition trade-off. Altogether, our data provide support for the mass-effect paradigm, where regional coexistence is mediated by specialization on different habitat types, and local coexistence by rescue effects from source sites. The strong regional dynamics and demographic stochasticity, together with high dispersal rates, presumably contributed to mass effects by overriding local differences in specific competitive abilities.

The effect of host social system on parasite population genetic structure: comparative population genetics of two ectoparasitic mites and their bat hosts.

BACKGROUND: The population genetic structure of a parasite, and consequently its ability to adapt to a given host, is strongly linked to its own life history as well as the life history of its host. While the effects of parasite life history on their population genetic structure have received some attention, the effect of host social system has remained largely unstudied. In this study, we investigated the population genetic structure of two closely related parasitic mite species (Spinturnix myoti and Spinturnix bechsteini) with very similar life histories. Their respective hosts, the greater mouse-eared bat (Myotis myotis) and the Bechstein's bat (Myotis bechsteinii) have social systems that differ in several substantial features, such as group size, mating system and dispersal patterns. RESULTS: We found that the two mite species have strongly differing population genetic structures. In S. myoti we found high levels of genetic diversity and very little pairwise differentiation, whereas in S. bechsteini we observed much less diversity, strongly differentiated populations and strong temporal turnover. These differences are likely to be the result of the differences in genetic drift and dispersal opportunities afforded to the two parasites by the different social systems of their hosts. CONCLUSIONS: Our results suggest that host social system can strongly influence parasite population structure. As a result, the evolutionary potential of these two parasites with very similar life histories also differs, thereby affecting the risk and evolutionary pressure exerted by each parasite on its host.