Ecological speciation is facilitated when divergent adaptation has direct effects on selective mating. Divergent sensory adaptation could generate such direct effects, by mediating both ecological performance and mate selection. In aquatic environments, light attenuation creates distinct photic environments, generating divergent selection on visual systems. Consequently, divergent sensory drive has been implicated in the diversification of several fish species. Here, we experimentally test whether divergent visual adaptation explains the divergence of mate preferences in Haplochromine cichlids. Blue and red Pundamilia co-occur across south-eastern Lake Victoria. They inhabit different photic conditions and have distinct visual system properties. Previously, we documented that rearing fish under different light conditions influences female preference for blue versus red males. Here, we examine to what extent variation in female mate preference can be explained by variation in visual system properties, testing the causal link between visual perception and preference. We find that our experimental light manipulations influence opsin expression, suggesting a potential role for phenotypic plasticity in optimizing visual performance. However, variation in opsin expression does not explain species differences in female preference. Instead, female preference covaries with allelic variation in the long-wavelength-sensitive opsin gene (LWS), when assessed under broad-spectrum light. Taken together, our study presents evidence for environmental plasticity in opsin expression and confirms the important role of colour perception in shaping female mate preferences in Pundamilia. However, it does not constitute unequivocal evidence for the direct effects of visual adaptation on assortative mating.
Abstract Sensory adaptation to the local environment can contribute to speciation. Aquatic environments are well suited for studying this process: The natural attenuation of light through water results in heterogeneous light environments, to which vision‐dependent species must adapt for communication and survival. Here, we study visual adaptation in sympatric Pundamilia cichlids from southeastern Lake Victoria. Species with blue or red male nuptial coloration co‐occur at many rocky islands but tend to be depth‐differentiated, entailing different visual habitats, more strongly at some islands than others. Divergent visual adaptation to these environments has been implicated as a major factor in the divergence of P. pundamilia and P. nyererei, as they show consistent differentiation in the long‐wavelength‐sensitive visual pigment gene sequence (LWS opsin). In addition to sequence variation, variation in the opsin gene expression levels may contribute to visual adaptation. We characterized opsin gene expression and LWS genotype across Pundamilia populations inhabiting turbid and clear waters, to examine how different mechanisms of visual tuning contribute to visual adaptation. As predicted, the short‐wavelength‐sensitive opsin (SWS2b) was expressed exclusively in a population from clear water. Contrary to prediction however, expression levels of the other opsins were species‐ and island‐dependent and did not align with species differences in LWS genotype. Specifically, in two locations with turbid water, the shallow‐water dwelling blue species expressed more LWS and less RH2A than the deeper‐dwelling red species, while the opposite pattern occurred in the two locations with clear water. Visual modeling suggests that the observed distribution of opsin expression profiles and LWS genotypes does not maximize visual performance, implying the involvement of additional visual tuning mechanisms and/or incomplete adaptation. OPEN RESEARCH BADGE This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://hdl.handle.net/10411/I1IUUQ.
Following multiple matings, sperm from different males compete for fertilization within the female reproductive tract. In many species, this competition results in an unequal sharing of paternity that favors the most recent mate, termed last male sperm precedence (LMSP). Much of our understanding of LMSP comes from studies in Drosophila melanogaster that focus on twice-mated females with standardized latencies between successive matings. Despite accumulating evidence indicating that females often mate with more than two males and exhibit variation in the latency between matings, the consequences of mating rate on LMSP are poorly understood. Here, we developed a paradigm utilizing D. melanogaster in which females remated at various time intervals with either two or three transgenic males that produce fluorescent sperm (green, red, or blue). This genetic manipulation enables paternity assessment of offspring and male-specific sperm fate examination in female reproductive tracts. We found that remating latency had no relationship with LMSP in females that mated with two males. However, LMSP was significantly reduced in thrice-mated females with short remating intervals; coinciding with reduced last-male sperm storage. Thus, female remating rate influences the relative share of paternity, the overall clutch paternity diversity, and ultimately the acquisition of indirect genetic benefits to potentially maximize female reproductive success.
The neurotransmitter serotonin (5-HT) plays a vital regulatory role in both the brain and gut. 5-HT is crucial for regulating mood in the brain as well as gastrointestinal motility and secretion peripherally. Alterations in 5-HT transmission have been linked to pathological symptoms in both intestinal and psychiatric disorders and selective 5-HT transporter (5-HTT) inhibitors, affecting the 5-HT system by blocking the 5-HT transporter (5-HTT) have been successfully used to treat CNS- and intestinal disorders. Humans that carry the short allele of the 5-HTT-linked polymorphic region (5-HTTLPR) are more vulnerable to adverse environmental stressors, in particular early life stress. Although, early life stress has been shown to alter the composition of the gut microbiota, it is not known whether a lower 5-HTT expression is also associated with an altered microbiome composition. To investigate this, male and female wild type (5-HTT+/+), heterozygous (5-HTT+/-), and knockout (5-HTT-/-) 5-HT transporter rats were maternally separated for 6 h a day from postnatal day 2 till 15. On postnatal day 21, fecal samples were collected and the impact of 5-HTT genotype and maternal separation (MS) on the microbiome was analyzed using high-throughput sequencing of the bacterial 16S rRNA gene. MS showed a shift in the ratio between the two main bacterial phyla characterized by a decrease in Bacteroidetes and an increase in Firmicutes. Interestingly, the 5-HTT genotype caused a greater microbal dysbiosis (microbial imbalance) compared with MS. A significant difference in microbiota composition was found segregating 5-HTT-/- apart from 5-HTT+/- and 5-HTT+/+ rats. Moreover, exposure of rats with 5-HTT diminished expression to MS swayed the balance of their microbiota away from homeostasis to 'inflammatory' type microbiota characterized by higher abundance of members of the gut microbiome including Desulfovibrio, Mucispirillum, and Fusobacterium, all of which are previously reported to be associated with a state of intestinal inflammation, including inflammation associated with MS and brain disorders like multiple depressive disorders. Overall, our data show for the first time that altered expression of 5-HTT induces disruptions in male and female rat gut microbes and these 5-HTT genotype-related disruptions are augmented when combined with early life stress.