Marcel P. Haesler

Inheritance of female mating preference in a sympatric sibling species pair of Lake Victoria cichlids: implications for speciation

Female mate choice has often been proposed to play an important role in cases of rapid speciation, in particular in the explosively evolved haplochromine cichlid species flocks of the Great Lakes of East Africa. Little, if anything, is known in cichlid radiations about the heritability of female mating preferences. Entirely sympatric distribution, large ecological overlap and conspicuous differences in male nuptial coloration, and female preferences for these, make the sister species Pundamilia pundamilia and P. nyererei from Lake Victoria an ideally suited species pair to test assumptions on the genetics of mating preferences made in models of sympatric speciation. Female mate choice is necessary and sufficient to maintain reproductive isolation between these species, and it is perhaps not unlikely therefore, that female mate choice has been important during speciation. A prerequisite for this, which had remained untested in African cichlid fish, is that variation in female mating preferences is heritable. We investigated mating preferences of females of these sister species and their hybrids to test this assumption of most sympatric speciation models, and to further test the assumption of some models of sympatric speciation by sexual selection that female preference is a single–gene trait. We find that the differences in female mating preferences between the sister species are heritable, possibly with quite high heritabilities, and that few but probably more than one genetic loci contribute to this behavioural speciation trait with no apparent dominance. We discuss these results in the light of speciation models and the debate about the explosive radiation of cichlid fishes in Lake Victoria.

Color Polymorphism and Predation in a Lake Victoria Cichlid Fish

Abstract Haplochromine cichlid fish have radiated into hundreds of species in East-African lakes, possibly driven by divergent sexual selection on body coloration. We studied the color polymorphic Lake Victoria cichlid Neochromis omnicaeruleus, in which a presumably ancestral phenotype with blue males and brown females co-occurs with two distinct classes of blotched phenotypes in both sexes. Similar blotch polymorphisms occur in other haplochromine species, and in all studied cases blotched females are much more common than blotched males. In N. omnicaeruleus, the near absence of blotched males seems to be partly due to genetic linkage to a dominant female determiner that turns blotched males into females. However, laboratory breeding suggests that blotched males should be much more common than observed. Here we studied whether differential predation on blotched males contributes to their scarcity. First, in a predation experiment with wild birds, blotched fish indeed incurred more predator attacks. Second, underwater observations revealed behavioral differences between the sexes, consistent with an additional predation risk for males. These data suggest that differential predation with regard to color pattern and sex may be an important selective force in the evolution and maintenance of this color polymorphism. However, we also carried out a population census which revealed that blotched males were rare already as juveniles. To explain the scarcity of blotched males in nature, we therefore have to invoke either selection against blotched males early in life, or a more complex genetic model. These results emphasize the need for further research on the ecology and genetics of this widespread color polymorphism in cichlid fish.

Establishment and expansion of Lake Malawi rock fish populations after a dramatic Late Pleistocene lake level rise

Major environmental events that fragment populations among multiple island habitats have potential to drive large‐scale episodes of speciation and adaptive radiation. A recent palaeolimnological study of sediment cores indicated that Lake Malawi underwent major climate‐driven desiccation events 75 000–135 000 years ago that lowered the water level to at least 580 m below the present state and severely reduced surface area. After this period, lake levels rose and stabilized, creating multiple discontinuous littoral rocky habitats. Here, we present evidence supporting the hypothesis that establishment and expansion of isolated philopatric rock cichlid populations occurred after this rise and stabilization of lake level. We studied the Pseudotropheus (Maylandia) species complex, a group with both allopatric and sympatric populations that differ in male nuptial colour traits and tend to mate assortatively. Using coalescent analyses based on mitochondrial DNA, we found evidence that populations throughout the lake started to expand and accumulate genetic diversity after the lake level rise. Moreover, most haplotypes were geographically restricted, and the greatest genetic similarities were typically among sympatric or neighbouring populations. This is indicative of limited dispersal and establishment of assortative mating among populations following the lake level rise. Together, this evidence is compatible with a single large‐scale environmental event being central to evolution of spatial patterns of genetic and species diversity in P. (Maylandia) and perhaps other Lake Malawi rock cichlids. Equivalent climate‐driven pulses of habitat formation and fragmentation may similarly have contributed to observed rapid and punctuated cladogenesis in other adaptive radiations.

Indirect mate choice, direct mate choice, and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand ‘bowers’. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co‐occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male‐mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.

When Phenotypes Do Not Match Genotypes—Unexpected Phenotypic Diversity and Potential Environmental Constraints in Icelandic Stickleback

Divergent lateral plate phenotypes in stickleback represent one of only a few cases known, where a single gene underlies the phenotype under divergent selection between different habitats. However, the selection pressures leading to the repeated loss of lateral plates in freshwater are still not well understood. By genotyping 838 individuals from 9 independently colonized lakes and 1 marine population in Iceland, we found 1) that only in some lakes are phenotypes associated with the expected genotype and 2) that the independent repeated occurrence of a rarely described plate phenotype is expressed in the absence of an allele that is usually associated with this phenotype. This suggests that either other genes such as modifiers might be under divergent selection between lakes or that lateral plate expression in these populations is restricted due to environmental constraints.

Little evidence for a selective advantage of armour-reduced threespined stickleback individuals in an invertebrate predation experiment

The repeated colonization of freshwater habitats by the ancestrally marine threespined stickleback Gasterosteus aculeatus has been associated with many instances of parallel reduction in armour traits, most notably number of lateral plates. The change in predation regime from marine systems, dominated by gape-limited predators such as piscivorous fishes, to freshwater habitats where grappling invertebrate predators such as insect larvae can dominate the predation regime, has been hypothesized as a driving force. Here we experimentally test the hypothesis that stickleback with reduced armour possess a selective advantage in the face of predation by invertebrates, using a natural population of stickleback that is highly polymorphic for armour traits and a common invertebrate predator from the same location. Our results provide no compelling evidence for selection in this particular predator–prey interaction. We suggest that the postulated selective advantage of low armour in the face of invertebrate predation may not be universal.

Reproductive parasitism: male and female responses to conspecific and heterospecific intrusions at spawning in a mouth-brooding cichlid Ophthalmotilapia ventralis.

A rare form of alternative reproductive behaviour without simultaneous parasitic spawning was observed in Ophthalmotilapia ventralis, a lekking mouth-brooding cichlid from Lake Tanganyika. Floater males attempted to sneak opportunistically into the territory to actively court the female, while the owner (bourgeois male) defended the territory against other potential intruders. Floater males had more body fat than territory owners and generally higher condition factors. In field experiments, the response of bourgeois males and courted females was tested towards floaters and egg predators (a catfish Synodontis multipunctatus) present in the territories. Territory owners responded aggressively particularly to floaters, and female responsiveness to bourgeois male courtship tended to decline when floaters were present. The potential influence of reproductive parasitism on sexual selection in mouth-brooding cichlids is discussed.

Genomic landscape of early ecological speciation initiated by selection on nuptial colour

Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment‐dependent sexual selection has played an important role. Here, we describe a very young (~90 years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat colour and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American west coast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat colour and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defence or swimming performance. Using genomewide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of colour. Our results suggest that phenotypic and multichromosome genomic divergence of these morphs was driven by environment‐dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry.

Pliocene isolation of a north-west Saharan cichlid fish

The evolutionary origin of the only north-west Saharan haplochromine cichlid, Astatotilapia desfontainii, was explored using mitochondrial DNA sequences. Phylogenetic analyses revealed that this species belonged to the main East African-Nilotic haplochromine clade, but was a distinct lineage that diverged from modern haplochromines in the Pliocene. The results suggest that A. desfontainii is a relict haplochromine lineage that has endured major climate fluctuations in North Africa.

A Dense Linkage Map of Lake Victoria Cichlids Improved the Pundamilia Genome Assembly and Revealed a Major QTL for Sex-Determination

Genetic linkage maps are essential for comparative genomics, high quality genome sequence assembly and fine scale quantitative trait locus (QTL) mapping. In the present study we identified and genotyped markers via restriction-site associated DNA (RAD) sequencing and constructed a genetic linkage map based on 1,597 SNP markers of an interspecific F2 cross of two closely related Lake Victoria cichlids (Pundamilia pundamilia and P. sp. ‘red head’). The SNP markers were distributed on 22 linkage groups and the total map size was 1,594 cM with an average marker distance of 1.01 cM. This high-resolution genetic linkage map was used to anchor the scaffolds of the Pundamilia genome and estimate recombination rates along the genome. Via QTL mapping we identified a major QTL for sex in a ∼1.9 Mb region on Pun-LG10, which is homologous to Oreochromis niloticus LG 23 (Ore-LG23) and includes a well-known vertebrate sex-determination gene (amh).