Rapid generation of ecologically relevant behavioral novelty in experimental cichlid hybrids.

The East African cichlid radiations are characterized by repeated and rapid diversification into many distinct species with different ecological specializations and by a history of hybridization events between nonsister species. Such hybridization might provide important fuel for adaptive radiation. Interspecific hybrids can have extreme trait values or novel trait combinations and such transgressive phenotypes may allow some hybrids to explore ecological niches neither of the parental species could tap into. Here, we investigate the potential of second-generation (F2) hybrids between two generalist cichlid species from Lake Malawi to exploit a resource neither parental species is specialized on: feeding by sifting sand. Some of the F2 hybrids phenotypically resembled fish of species that are specialized on sand sifting. We combined experimental behavioral and morphometric approaches to test whether the F2 hybrids are transgressive in both morphology and behavior related to sand sifting. We then performed a quantitative trait loci (QTL) analysis using RADseq markers to investigate the genetic architecture of morphological and behavioral traits. We show that transgression is present in several morphological traits, that novel trait combinations occur, and we observe transgressive trait values in sand sifting behavior in some of the F2 hybrids. Moreover, we find QTLs for morphology and for sand sifting behavior, suggesting the existence of some loci with moderate to large effects. We demonstrate that hybridization has the potential to rapidly generate novel and ecologically relevant phenotypes that may be suited to a niche neither of the parental species occupies. Interspecific hybridization may thereby contribute to the rapid generation of ecological diversity in cichlid radiations

Contrasting signatures of genomic divergence during sympatric speciation

Population genomic analyses of Midas cichlid fishes in young Nicaraguan crater lakes suggest that sympatric speciation is promoted by polygenic architectures. The transition from 'well-marked varieties' of a single species into 'well-defined species'-especially in the absence of geographic barriers to gene flow (sympatric speciation)-has puzzled evolutionary biologists ever since Darwin(1,2). Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process(3). Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs(4), but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories(5). Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.Peer reviewe

Patterns and process during the diversification of the cichlid fishes in Lake Malawi, Africa

The 500-1000 cichlid species endemic to Lake Malawi constitute one of the most rapid and extensive radiations of vertebrates ever discovered. The objective of this dissertation was to test the assumptions and predictions of several recently published models of cichlid speciation. First, a novel assay of female choice was used to evaluate the role of visual cues during conspecific recognition. The results of this experiment demonstrate that females are able to identify conspecific mates using only visual cues. Second, the assumptions of a recent model of speciation via intrasexual selection were tested by comparing aggressive behavior during territorial contests among five closely related cichlid species from Lake Malawi. I found that interactions between conspicuously heteromorphic males tend to be less aggressive than between those of homomorphic males. Third, I used transect data to evaluate the intrinsic and extrinsic factors that have affected the dispersal of 17 closely related cichlid species introduced to Thumbi West Island in Lake Malawi. A quarter of a century after their initial introduction, I found that the translocated cichlid community around Thumbi West Island is still in a state of flux, as many species continue to spread around the island. Next, I evaluated the patterns of divergence predicted by three competing speciation models that differ in the temporal action of natural and sexual selection by using AFLP to reconstruct the evolutionary relationships among 20 species of the ubiquitous rock dwelling subgenus Pseudotropheus tropheops. I found that cladogenesis is associated with numerous unambiguous changes in male color states. A geometric morphometric analysis of the lower jaw of these taxa revealed that the repeated differentiation of jaw morphology is associated with species habitat preference. Finally, I used AFLP data to reconstruct the evolution of species within three genera of sand dwelling cichlids that construct elaborate male display platforms. I found that sister taxa with distinct bower morphologies, and that exist in discrete leks separated by only 1-2m of depth, are divergent in both sexually selected and ecological traits. These phylogenies suggest that the forces of sexual and ecological selection have been intertwined during the speciation of these groups

Populations genetically rifting within a complex geological system: the case of strong structure and low genetic diversity in the migratory freshwater catfish, Bagrus docmak, in East Africa

The complex geological history of East Africa has been a driving factor in the rapid evolution of teleost biodiversity. While there is some understanding of how macroevolutionary drivers have shaped teleost speciation in East Africa, there is a paucity of research into how the same biogeographical factors have affected microevolutionary processes within lakes and rivers. To address this deficiency, population genetic diversity, demography, and structure were investigated in a widely distributed and migratory (potamodromous) African teleost species, Ssemutundu (Bagrus docmak). Samples were acquired from five geographical locations in East Africa within two major drainage basins; the Albertine Rift and Lake Victoria Basin. Individuals (N = 175) were genotyped at 12 microsatellite loci and 93 individuals sequenced at the mitochondrial DNA control region. Results suggested populations from Lakes Edward and Victoria had undergone a severe historic bottleneck resulting in very low nucleotide diversity (π = 0.004 and 0.006, respectively) and negatively significant Fu values (−3.769 and −5.049; p < .05). Heterozygosity deficiencies and restricted effective population size (NeLD) suggested contemporary exposure of these populations to stress, consistent with reports of the species decline in the East African Region. High genetic structuring between drainages was detected at both historical (ɸST = 0.62 for mtDNA; p < .001) and contemporary (microsatellite FST = 0.460; p < .001) levels. Patterns of low genetic diversity and strong population structure revealed are consistent with speciation patterns that have been linked to the complex biogeography of East Africa, suggesting that these biogeographical features have operated as both macro- and micro-evolutionary forces in the formation of the East African teleost fauna

Interspecific Genetic Differences and Historical Demography in South American Arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum)

The South American arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum) are emblematic species widely distributed in the Amazon and surrounding basins. Arowana species are under strong anthropogenic pressure as they are extensively exploited for ornamental and food purposes. Until now, limited genetic and cytogenetic information has been available, with only a few studies reporting to their genetic diversity and population structure. In the present study, cytogenetic and DArTseq-derived single nucleotide polymorphism (SNP) data were used to investigate the genetic diversity of the two Osteoglossum species, the silver arowana O. bicirrhosum, and the black arowana O. ferreirai. Both species differ in their 2n (with 2n = 54 and 56 for O. ferreirai and O. bicirrhosum, respectively) and in the composition and distribution of their repetitive DNA content, consistent with their taxonomic status as different species. Our genetic dataset was coupled with contemporary and paleogeographic niche modeling, to develop concurrent demographic models that were tested against each other with a deep learning approach in O. bicirrhosum. Our genetic results reveal that O. bicirrhosum colonized the Tocantins-Araguaia basin from the Amazon basin about one million years ago. In addition, we highlighted a higher genetic diversity of O. bicirrhosum in the Amazon populations in comparison to those from the Tocantins-Araguaia basin. © 2019 by the authors. Licensee MDPI, Basel, Switzerland

The effects of eutrophication on alternative reproductive tactics in threespine sticklebacks

When organisms compete for mates and fertilisations, the process of sexual selection drives the evolution of traits that increase reproductive success. The traits targeted by selection, and the extent to which they change, are constrained by the local environment. Sexual selection due to female mate choice can be undermined by alternative reproductive tactics (ARTs), which refers to discontinuous variation in traits or behaviours used in reproduction. As human activities are rapidly changing our planet, this raises the question how ARTs will be affected. Fish show a bewildering diversity of ARTs, which make them good model organisms to answer these questions. One example of human-induced environmental change, which is affecting aquatic ecosystems around the world, is eutrophication, the over-enrichment of water bodies with nutrients. One of its effects is decreased underwater visibility due to increases in both turbidity and vegetation density. The aims of this thesis were to investigate the effects increased turbidity and vegetation density have on an ART in sticklebacks, a fish common to marine and fresh water bodies of the Northern hemisphere. I furthermore investigated how this affected sexual selection for male size, a trait commonly under selection. I used a combination of behavioural observations in microcosms, where I manipulated underwater visibility, with collection of genetic material to reconstruct parentage of broods, and thus identify sneak fertilisations. The results show that turbidity might have weak negative effects on the frequency of sneaking behaviour, although this behaviour was rather infrequent in these experiments, which complicates firm conclusions. In dense vegetation the number of sneak fertilisations decreased slightly, as fewer nesting males sneaked, while the number of non-nesting males sneaking remained constant. The paternity analyses revealed that a significantly smaller fraction of eggs was sneak fertilised under dense vegetation. Furthermore, amongst the nesting males that sneaked, the amount of eggs sneak fertilised correlated positively with courtship success. A reduction in sneaking by these males under dense vegetation equalised the distribution of fertilisation success, in turn contributing to a decrease in the opportunity for selection. Under dense vegetation significantly more males built nests, which has also been observed in previous field studies. In a separate experiment we addressed if such changes in the proportion of nesters and non-nesters, without changes in visibility, affected the incidence of sneak fertilisation. My results show this was not the case, likely because sneaking is an opportunistic tactic shown by both nesters and non-nesters. Non-nesters did sneak proportionately more when there were many of them, which could be due to changes in the cost-benefit ratio of sneaking. As nesters can only attack one intruder at a time, the costs and risks per sneaker will decrease as the number of sneakers increases. The defensive behaviours shown by the nesters before spawning shifted to a more aggressive form of nest defence. This could be because less aggressive behaviours lose their effectiveness when the number of intruders increases. It could also indicate that the risks associated with aggressive behaviours decrease when there are fewer fellow nesters, as other studies indicate nesters are competitive and aggressive individuals. Under turbid conditions I did not detect changes in the opportunity for selection, based on fertilisation success, nor was male size under significant selection under clear or turbid conditions. More thorough analyses under densely vegetated conditions across the nesting, courtship and fertilisation stages revealed a decrease in the opportunity for selection across all stages. A reduction in sneaking by nesters contributed to this. During the nesting stage, but not during later stages, body size was under significant directional selection under sparse, but not dense vegetation. This illustrates the importance of considering all selection stages to get a complete picture of how environmental changes affect sexual selection. Leaving out certain stages or subgroups can result in incomplete or misleading results.Kilpailu parittelukumppaneista voi johtaa liioiteltuihin ja prameileviin ominaisuuksiin niin nisäkkäillä, kaloilla, linnuilla kuin monilla muillakin organismeilla (esimerkkinä riikinkukon pyrstö ja peuran sarvet). Korea ulkomuoto ei kuitenkaan ole ainut tapa varmistaa kumppanin löytyminen ja omien geenien siirtyminen eteenpäin. Niin kutsutut vaihtoehtoiset lisääntymistaktiikat mahdollistavat lisääntymismenestyksen eri reittiä. Kalamaailman esimerkki vaihtoehtoisesta lisääntymistaktiikasta on niin sanottu "hiiviskelyhedelmöitys"(sneak fertilisation). Useilla kalalajeilla koiraat valtaavat reviirin, rakentavat pesän ja houkuttelevat naaraita paikalle kutemaan. Kaikki koiraat eivät kuitenkaan rakenna pesää: joukosta löytyy myös huijareita, ns. "hiiviskelijöitä" (sneaker). Nämä koirasyksilöt piileskelevät naapurinsa pesän kulmalla ja rientävät heti pesänomistajan silmän välttäessä kutemaan paikalle saapuneen naaraan kanssa. Lisääntymismenestykselle ja vaihtoehtoisille taktiikoille tärkeät ominaisuudet ovat alttiita ympäristönmuutoksille. Yksi Itämeren suurimmista ympäristöongelmista on rehevöityminen. Rehevöitymisen syynä ovat lisääntyneet ravinnemäärät vedessä. Ravinteet voivat olla lähtöisin esimerkiksi jätevesistä tai maatalouden päästöistä. Rehevöityneissä vesissä kausittaiset leväkukinnot ovat runsaampia ja vesi sameampaa. Tämä puolestaan vaikuttaa näkyvyyteen vedessä ja voi siten haitata eri lisääntymistaktiikoiden toimivuutta. Tutkin vaihtoehtoisia lisääntymistaktiikoita kolmipiikillä, joka on yleinen Itämeren pikkukala. Kolmipiikkikoiraat rakentavat pesän ja houkuttelevat naaraan paikalle kutemaan, mutta koiraiden joukosta löytyy myös hiiviskelijöitä. Tein useita allas- ja akvaariokokeita näillä kaloilla muunnellen veden sameutta ja tarkkaillen kalojen käyttäytymistä. Keräsin myös geneettistä aineistoa, jonka avulla selvitin kuka hedelmöitti naaraan munat ja kuinka menestyksekkäitä tunkeilijat olivat. Tulokseni osoittavat, että veden sameus voi vähentää hiiviskelyn todennäköisyyttä, mutta vaikutus ei ole kovin voimakas. Leväkasvillisuuden lisääntyminen vähensi myös hiiviskelyllä hedelmöitettyjen munien määrää ja erityisesti pesivien koiraiden hiiviskelyn osuutta. Tiheässä kasvillisuudessa yhä useampi koiras kykeni rakentamaan pesän, mikä todennäköisesti johtuu siitä, että lisääntynyt leväkasvillisuus vähentää koiraiden kohtaamisia ja siten kilpailun määrää. Lisääntyminen muuttui tilanteesta, jossa harvat koiraat rakensivat pesän ja samalla hankkivat lisää jälkeläisiä hiiviskelemällä muiden pesille, tilanteeseen, jossa useilla koirailla on pesä, mutta hiiviskelyn osuus vähenee. Tällaisessa tilanteessa kaikenkokoiset koiraat pääsivät kutemaan ja koiraan koon merkitys lisääntymismenestyksen kannalta väheni. Erillisessä kokeessa tutkin, miten pesivien ja pesättömien koiraiden määrän vaihtelu vaikuttaa hiiviskelyn todennäköisyyteen. Vaikutusta ei löytynyt, sillä hiiviskely on kolmipiikeillä opportunistinen taktiikka, jota harjoittavat sekä pesivät että pesättömät koiraat. Hiiviskely antaa koiraille mahdollisuuden vähentää naaraiden valinnan merkitystä: vähemmän suositut koiraat pääsevät hiiviskelemällä myös lisääntymään. Jos hiiviskelyn määrä rehevissä elinympäristöissä vähenee, mihin tulokseni viittaavat, tämä tarkoittaisi naaraan valinnan merkityksen voimistumista. Tilanne ei kuitenkaan ole niin yksinkertainen, sillä geneettinen aineisto osoittaa, että suositut koiraat, joilla on jo pesä, vastaavat myös isosta osasta hiiviskelyä. Rehevöitymisen aiheuttama huonontunut näkyvyys voi siis vähentää naaraan valinnan vaikutusta, sillä yhä harvempi suosittu koiras enää panostaa tuleviin sukupolviin. Nämä tulokset ovat samassa linjassa aiempien tällä lajilla tehtyjen tutkimusten kanssa: rehevöityminen muuttaa lisääntymisjärjestelmää ja heikentää jo olemassa olevien preferenssien merkitystä. Muutokset hiiviskelykäyttäytymisessä voivat osaltaan vaikuttaa tähän. Lisätutkimukset aiheen piirissä ovat tarpeen vahvistamaan jo saamiani tuloksia, etenkin kenttäolosuhteissa, jotta havaitsemieni käyttäytymismuutosten paikkansapitävyys voitaisiin todeta myös luonnonolosuhteissa

A brain and a head for a different habitat : Size variation in four morphs of Arctic charr (Salvelinus alpinus(L.)) in a deep oligotrophic lake

Adaptive radiation is the diversification of species to different ecological niches and has repeatedly occurred in different salmonid fish of postglacial lakes. In Lake Tinnsjoen, one of the largest and deepest lakes in Norway, the salmonid fish, Arctic charr (Salvelinus alpinus(L.)), has likely radiated within 9,700 years after deglaciation into ecologically and genetically segregated Piscivore, Planktivore, Dwarf, and Abyssal morphs in the pelagial, littoral, shallow-moderate profundal, and deep-profundal habitats. We compared trait variation in the size of the head, the eye and olfactory organs, as well as the volumes of five brain regions of these four Arctic charr morphs. We hypothesised that specific habitat characteristics have promoted divergent body, head, and brain sizes related to utilized depth differing in environmental constraints (e.g., light, oxygen, pressure, temperature, and food quality). The most important ecomorphological variables differentiating morphs were eye area, habitat, and number of lamellae. The Abyssal morph living in the deepest areas of the lake had the smallest brain region volumes, head, and eye size. Comparing the olfactory bulb with the optic tectum in size, it was larger in the Abyssal morph than in the Piscivore morph. The Piscivore and Planktivore morphs that use more illuminated habitats have the largest optic tectum volume, followed by the Dwarf. The observed differences in body size and sensory capacities in terms of vision and olfaction in shallow and deepwater morphs likely relates to foraging and mating habitats in Lake Tinnsjoen. Further seasonal and experimental studies of brain volume in polymorphic species are needed to test the role of plasticity and adaptive evolution behind the observed differences.Peer reviewe

Intragenus F1-hybrids of African weakly electric fish (Mormyridae: Campylomormyrus tamandua ♂ × C. compressirostris ♀) are fertile

Hybridization is widespread in fish and constitutes an important mechanism in fish speciation. There is, however, little knowledge about hybridization in mormyrids. F1-interspecies hybrids between Campylomormyrus tamandua ♂ × C. compressirostris ♀ were investigated concerning: (1) fertility; (2) survival of F2-fish and (3) new gene combinations in the F2-generation concerning the structure of the electric organ and features of the electric organ discharge. These F1-hybrids achieved sexual maturity at about 12–13.5 cm total length. A breeding group comprising six males and 13 females spawned 28 times naturally proving these F1-fish to be fertile. On average 228 eggs were spawned, the average fertilization rate was 47.8%. Eggs started to hatch 70–72 h after fertilization, average hatching rate was 95.6%. Average mortality rate during embryonic development amounted to 2.3%. Average malformation rate during the free embryonic stage was 27.7%. Exogenous feeding started on day 11. In total, we raised 353 normally developed larvae all of which died consecutively, the oldest specimen reaching an age of 5 months. During survival, the activities of the larval and adult electric organs were recorded and the structure of the adult electric organ was investigated histologically.Peer Reviewe

Investigation of sympatric speciation as the outcome of competition for food resource by means of an individual-based modeling approach

Sympatric speciation, the emergence of new species in the absence of geographic isolation, is one of the most controversial issues in evolutionary biology. Although today the plausibility of the occurrence of sympatric speciation is theoretically acknowledged, its underlying mechanisms are still unknown. We applied a modeling approach with three trophic levels (primary resource, prey, and predator) and supplied prey species with two different food resources (Food 1 and Food 2) to track prey lineage through evolutionary time to detect any indicators of the occurrence of sympatric speciation caused by specialized food consumption. Whereas, Food 1 was the more available resource, Food 2 had higher energy content. Initially, when there was not yet any specific food specialization, Food 1 consumption rate was significantly higher compared to Food 2. Eventually, around time step 22,000 and after the emergence of food consumption specialization, the exploitation of Food 2 was higher than Food 1 in spite of the fact that prey individuals were more frequently encountered with Food 1 than Food 2. Drawing a comparison between simulations with only one food resource and simulations with two available food resources revealed that complete reproductive isolation caused by disruptive selective pressure exerted by adaptation to different resources plays a curial role in the emergence of sympatric species. Machine learning techniques were also employed to identify the shared patterns among sympatric species. Results showed that for most lineages sympatric divergence has occurred at the beginning of the process of the emergence of specialized use. If not, these species have possessed a high spatial distribution and had to meet two conditions to be diverged sympatrically: i. high genetic diversity and ii. a large population size