Alloparental care between catfishes in Lake Tanganyika

A bagrid catfish Auchenoglanis occidentalis cared for its brood, deposited within an accumulation of shells and gravel in the centre of a large saucer-like depression, for up to 2 weeks in Lake Tanganyika. Adults of another catfish Dinotopterus cunningtoni (Clariidae) persistently came to A. occidentalis nests near days of host spawning. Eggs of D. cunningtoni were found in the host nests on the day and within 2 days of host spawning. During and for a few days after the end of host brooding, associate species' young of much older ages than the host brood were often found in the nests together with those of a similar age to the host young. Associate young were rarely found in nests before spawning and in unused nests. These findings suggested that this brood-mixing has two origins: egg dumping by associate adults and voluntary intrusion of large associate young into host nests. Possible benefits to the associate species are to take advantage of nest preparation and parental behaviour of the host species and to feed on the host brood.     

Adaptive divergence between lake and stream populations of an East African cichlid fish

Divergent natural selection acting in different habitats may build up barriers to gene flow and initiate speciation. This speciation continuum can range from weak or no divergence to strong genetic differentiation between populations. Here, we focus on the early phases of adaptive divergence in the East African cichlid fish Astatotilapia burtoni, which occurs in both Lake Tanganyika (LT) and inflowing rivers. We first assessed the population structure and morphological differences in A. burtoni from southern LT. We then focused on four lake–stream systems and quantified body shape, ecologically relevant traits (gill raker and lower pharyngeal jaw) as well as stomach contents. Our study revealed the presence of several divergent lake–stream populations that rest at different stages of the speciation continuum, but show the same morphological and ecological trajectories along the lake–stream gradient. Lake fish have higher bodies, a more superior mouth position, longer gill rakers and more slender pharyngeal jaws, and they show a plant/algae and zooplankton‐biased diet, whereas stream fish feed more on snails, insects and plant seeds. A test for reproductive isolation between closely related lake and stream populations did not detect population‐assortative mating. Analyses of F1 offspring reared under common garden conditions indicate that the detected differences in body shape and gill raker length do not constitute pure plastic responses to different environmental conditions, but also have a genetic basis. Taken together, the A. burtoni lake–stream system constitutes a new model to study the factors that enhance and constrain progress towards speciation in cichlid fishes.     

Niche divergence promotes rapid diversification of East African sky island white‐eyes (Aves: Zosteropidae)

The Eastern Afromontane biodiversity hotspot composed of highly fragmented forested highlands (sky islands) harbours exceptional diversity and endemicity, particularly within birds. To explain their elevated diversity within this region, models founded on niche conservatism have been offered, although detailed phylogeographic studies are limited to a few avian lineages. Here, we focus on the recent songbird genus Zosterops, represented by montane and lowland members, to test the roles of niche conservatism versus niche divergence in the diversification and colonization of East Africa's sky islands. The species‐rich white‐eyes are a typically homogeneous family with an exceptional colonizing ability, but in contrast to their diversity on oceanic islands, continental diversity is considered depauperate and has been largely neglected. Molecular phylogenetic analysis of ~140 taxa reveals extensive polyphyly among different montane populations of Z. poliogastrus. These larger endemic birds are shown to be more closely related to taxa with divergent habitat types, altitudinal distributions and dispersal abilities than they are to populations of restricted endemics that occur in neighbouring montane forest fragments. This repeated transition between lowland and highland habitats over time demonstrate that diversification of the focal group is explained by niche divergence. Our results also highlight an underestimation of diversity compared to morphological studies that has implications for their taxonomy and conservation. Molecular dating suggests that the spatially extensive African radiation arose exceptionally rapidly (1–2.5 Ma) during the fluctuating Plio‐Pleistocene climate, which may have provided the primary driver for lineage diversification.     

Contrasting geographic structure in evolutionarily divergent Lake Tanganyika catfishes

Geographic isolation is suggested to be among the most important processes in the generation of cichlid fish diversity in East Africa's Great Lakes, both through isolation by distance and fluctuating connectivity caused by changing lake levels. However, even broad scale phylogeographic patterns are currently unknown in many non‐cichlid littoral taxa from these systems. To begin to address this, we generated restriction‐site‐associated DNA sequence (RADseq) data to investigate phylogeographic structure throughout Lake Tanganyika (LT) in two broadly sympatric rocky shore catfish species from independent evolutionary radiations with differing behaviors: the mouthbrooding claroteine, Lophiobagrus cyclurus, and the brood‐parasite mochokid, Synodontis multipunctatus. Our results indicated contrasting patterns between these species, with strong lake‐wide phylogeographic signal in L. cyclurus including a deep divergence between the northern and southern lake basins. Further structuring of these populations was observed across a heterogeneous habitat over much smaller distances. Strong population growth was observed in L. cyclurus sampled from shallow shorelines, suggesting population growth associated with the colonization of new habitats following lake‐level rises. Conversely, S. multipunctatus, which occupies a broader depth range, showed little phylogeographic structure and lower rates of population growth. Our findings suggest that isolation by distance and/or habitat barriers may play a role in the divergence of non‐cichlid fishes in LT, but this effect varies by species.     

Persistence of host defence behaviour in the absence of avian brood parasitism

The fate of host defensive behaviour in the absence of selection from brood parasitism is critical to long-term host-parasite coevolution. We investigated whether New World Bohemian waxwings Bombycilla garrulus that are allopatric from brown-headed cowbird Molothrus ater and common cuckoo Cuculus canorus parasitism have retained egg rejection behaviour. We found that egg rejection was expressed by 100 per cent of Bohemian waxwings. Our phylogeny revealed that Bohemian and Japanese waxwings Bombycilla japonica were sister taxa, and this clade was sister to the cedar waxwing Bombycilla cedrorum. In addition, there was support for a split between Old and New World Bohemian waxwings. Our molecular clock estimates suggest that egg rejection may have been retained for 2.8-3.0 Myr since New World Bohemian waxwings inherited it from their common ancestor with the rejecter cedar waxwings. These results support the 'single trajectory' model of host-brood parasite coevolution that once hosts evolve defences, they are retained, forcing parasites to become more specialized over time.     

A single ancient origin of brood parasitism in African finches: implications for host-parasite coevolution

Robust phylogenies for brood-parasitic birds, their hosts, and nearest nesting relatives provide the framework to address historical questions about host-parasite coevolution and the origins of parasitic behavior. We tested phylogenetic hypotheses for the two genera of African brood-parasitic finches, Anomalospiza and Vidua, using mitochondrial DNA sequence data from 43 passeriform species. Our analyses strongly support a sister relationship between Vidua and Anomalospiza, leading to the conclusion that obligate brood parasitism evolved only once in African finches rather than twice, as has been the conventional view. In addition, the parasitic finches (Viduidae) are not recently derived from either weavers (Ploceidae) or grassfinches (Estrildidae), but represent a third distinct lineage. Among these three groups, the parasitic finches and estrildids, which includes the hosts of all 19 Vidua species, are sister taxa in all analyses of our full dataset. Many characters shared by Vidua and estrildids, including elaborate mouth markings in nestlings, unusual begging behavior, and immaculate white eggs, can therefore be attributed to common ancestry rather than convergent evolution. The host-specificity of mouth mimicry in Vidua species, however, is clearly the product of subsequent host-parasite coevolution. The lineage leading to Anomalospiza switched to parasitizing more distantly related Old World warblers (Sylviidae) and subsequently lost these characteristics. Substantial sequence divergence between Vidua and Anomalospiza indicates that the origin of parasitic behavior in this clade is ancient (approximately 20 million years ago), a striking contrast to the recent radiation of extant Vidua. We suggest that the parasitic finch lineage has experienced repeated cycles of host colonization, speciation, and extinction through their long history as brood parasites and that extant Vidua species represent only the latest iterations of this process. This dynamic process may account for a significantly faster rate of DNA sequence evolution in parasitic finches as compared to estrildids and other passerines. Our study reduces by one the tally of avian lineages in which obligate brood parasitism has evolved and suggests an origin of parasitism that involved relatively closely related species likely to accept and provide appropriate care to parasitic young. Given the ancient origin of parasitism in African finches, ancestral estrildids must have been parasitized well before the diversification of extant Vidua, suggesting a long history of coevolution between these lineages preceding more recent interactions between specific hosts and parasites.     

Parallelism in adaptive radiations of experimental Escherichia coli populations

Adaptive radiations are major contributors to species diversity. Although the underlying mechanisms of adaptive radiations, specialization and trade‐offs, are relatively well understood, the tempo and repeatability of adaptive radiations remain elusive. Ecological specialization can occur through the expansion into novel niches or through partitioning of an existing niche. To test how the mode of resource specialization affects the tempo and repeatability of adaptive radiations, we selected replicate bacterial populations in environments that promoted the evolution of diversity either through niche expansion or through niche partitioning, and in a third low‐quality single‐resource environment, in which diversity was not expected to evolve. Colony size diversity evolved equally fast in environments that provided ecological opportunities regardless of the mode of resource specialization. In the low‐quality environments, diversity did not consistently evolve. We observed the largest fitness improvement in the low‐quality environment and the smallest the glucose‐limited environment. We did not observe a change in the rate of evolutionary change in either trait or environment, suggesting that the pool of beneficial mutations was not exhausted. Overall, the mode of resource specialization did not affect the tempo or repeatability of adaptive radiations. These results demonstrate the limitations of eco‐evolutionary feedbacks to affect evolutionary outcomes.     

Temporally consistent species differences in parasite infection but no evidence for rapid parasite‐mediated speciation in Lake Victoria cichlid fish

Parasites may have strong eco‐evolutionary interactions with their hosts. Consequently, they may contribute to host diversification. The radiation of cichlid fish in Lake Victoria provides a good model to study the role of parasites in the early stages of speciation. We investigated patterns of macroparasite infection in a community of 17 sympatric cichlids from a recent radiation and 2 older species from 2 nonradiating lineages, to explore the opportunity for parasite‐mediated speciation. Host species had different parasite infection profiles, which were only partially explained by ecological factors (diet, water depth). This may indicate that differences in infection are not simply the result of differences in exposure, but that hosts evolved species‐specific resistance, consistent with parasite‐mediated divergent selection. Infection was similar between sampling years, indicating that the direction of parasite‐mediated selection is stable through time. We morphologically identified 6 Cichlidogyrus species, a gill parasite that is considered a good candidate for driving parasite‐mediated speciation, because it is host species‐specific and has radiated elsewhere in Africa. Species composition of Cichlidogyrus infection was similar among the most closely related host species (members of the Lake Victoria radiation), but two more distantly related species (belonging to nonradiating sister lineages) showed distinct infection profiles. This is inconsistent with a role for Cichlidogyrus in the early stages of divergence. To conclude, we find significant interspecific variation in parasite infection profiles, which is temporally consistent. We found no evidence that Cichlidogyrus‐mediated selection contributes to the early stages of speciation. Instead, our findings indicate that species differences in infection accumulate after speciation.     

Gene expression remodelling and immune response during adaptive divergence in an African cichlid fish

Variation in gene expression contributes to ecological speciation by facilitating population persistence in novel environments. Likewise, immune responses can be of relevance in speciation driven by adaptation to different environments. Previous studies examining gene expression differences between recently diverged ecotypes have often relied on only one pair of populations, targeted the expression of only a subset of genes or used wild‐caught individuals. Here, we investigated the contribution of habitat‐specific parasites and symbionts and the underlying immunological abilities of ecotype hosts to adaptive divergence in lake–river population pairs of the cichlid fish Astatotilapia burtoni. To shed light on the role of phenotypic plasticity in adaptive divergence, we compared parasite and microbiota communities, immune response, and gene expression patterns of fish from natural habitats and a lake‐like pond set‐up. In all investigated population pairs, lake fish were more heavily parasitized than river fish, in terms of both parasite taxon composition and infection abundance. The innate immune response in the wild was higher in lake than in river populations and was elevated in a river population exposed to lake parasites in the pond set‐up. Environmental differences between lake and river habitat and their distinct parasite communities have shaped differential gene expression, involving genes functioning in osmoregulation and immune response. Most changes in gene expression between lake and river samples in the wild and in the pond set‐up were based on a plastic response. Finally, gene expression and bacterial communities of wild‐caught individuals and individuals acclimatized to lake‐like pond conditions showed shifts underlying adaptive phenotypic plasticity.     

A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite

Avian brood parasites reduce the reproductive output of their hosts and thereby select for defence mechanisms such as ejection of parasitic eggs. Such defence mechanisms simultaneously select for counter-defences in brood parasites, causing a coevolutionary arms race. Although coevolutionary models assume that defences and counter-defences are genetically influenced, this has never been demonstrated for brood parasites. Here, we give strong evidence for genetic differences between ejector and nonejectors, which could allow the study of such host defence at the genetic level, as well as studies of maintenance of genetic variation in defences. Briefly, we found that magpies, that are the main host of the great spotted cuckoo in Europe, have alleles of one microsatellite locus (Ase64) that segregate between accepters and rejecters of experimental parasitic eggs. Furthermore, differences in ejection rate among host populations exploited by the brood parasite covaried significantly with the genetic distance for this locus.