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Male phenotypes, light gradients and LWS opsin absorbance.a, Variation in male nuptial colouration. Five phenotype classes from 0 ('blue', typical P. pundamilia; top) to 4 ('red', typical P. nyererei; bottom). b, An example of a moderately steep light gradient (Python island): surface light spectrum (blue) and three subsurface light spectra measured at 0.5 m (green), 1.5 m (orange) and 2.5 m (red) water depth. The line through 550 nm indicates the divide used to calculate the transmittance orange ratio. Arrows indicate peak absorbance of two opsin pigments: main allele groups at LWS opsin locus (544 nm and 559 nm) and known range of peak absorbance at SWS2A locus16. c, Slopes of seven different light gradients. The lines for two shallow gradients overlay each other and are together labelled 'Mwanza Gulf'. For this line, the x-axis represents the distance from clear water (rather than from shore). Significant differentiation in opsin genes was observed on all gradients with slopes equal to or shallower than the Kissenda (orange) line, but speciation was observed only on gradients with slopes between the Kissenda (orange) and the Makobe (blue) lines. The dark grey arrow indicates region with divergent adaption at LWS opsin gene, and the light grey arrow indicates region with speciation. d, Absorption spectra of LWS pigments evaluated by the dark–light difference spectra9. The LWS pigments were reconstituted from the H allele with A1 retinal (top) and from the P allele with A1 retinal (bottom). max values (with standard errors) are indicated.
Source publication
Theoretically, divergent selection on sensory systems can cause speciation through sensory drive. However, empirical evidence is rare and incomplete. Here we demonstrate sensory drive speciation within island populations of cichlid fish. We identify the ecological and molecular basis of divergent evolution in the cichlid visual system, demonstrate...
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... in this study). The cichlids we study feed and breed right above and within the rocky substrate. We characterize depth-associated light gradients in their habitat by the change in the 'transmittance orange ratio' that occurs per metre as one moves outwards from the shore into the lake along the lake floor (the 'light slope', see Methods and Fig. 1b). Steeper slopes occur with more turbid water and steeper shores ( Table 1). The steepest light slopes occurred at the most turbid sites, Marumbi and Luanso islands (Table 1 and Fig. 1c). Intermediate slopes occurred at Kissenda and Python islands, and the shallowest slope at Makobe island. The latter was still steeper than all the ...
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... the 'transmittance orange ratio' that occurs per metre as one moves outwards from the shore into the lake along the lake floor (the 'light slope', see Methods and Fig. 1b). Steeper slopes occur with more turbid water and steeper shores ( Table 1). The steepest light slopes occurred at the most turbid sites, Marumbi and Luanso islands (Table 1 and Fig. 1c). Intermediate slopes occurred at Kissenda and Python islands, and the shallowest slope at Makobe island. The latter was still steeper than all the turbidity-mediated light slopes of our earlier work 9 . The size of the light differential between the ends of the gradients was similar between the five depth-mediated gradients, and ...
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... levels of differences between islands in the divergence between red and blue reported as P values of G-tests. b, Frequency distributions of male nuptial colour phenotypes (see Fig. 1a Table ...
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... reconstituted the LWS pigments from P alleles in vitro with A1- derived retinal, and measured their absorption spectra, as previously done for the H alleles 9 (Fig. 1d). The peak spectral sensitivity (l max ) of the A1 pigment of the P allele was blue-shifted by 15 nm relative to the H allele. The l max values of cone outer segments expressing either P or H pigments were measured previously by microspectrophoto- metry, reporting too that P pigments were blue-shifted relative to H pigments 16 . Hence, ...
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... l max values of cone outer segments expressing either P or H pigments were measured previously by microspectrophoto- metry, reporting too that P pigments were blue-shifted relative to H pigments 16 . Hence, the absorption spectra of P and H alleles seem to be adapted to shallower and deeper water light environments in Lake Victoria, respectively (Fig. 1b, d), supporting prediction ...
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... the exception of Makobe island, all microsatellite F ST among sympatric red and blue phenotypes are smaller than F ST between any two allopatric populations of the blue phenotype, and 7 out of 10 of the red phenotype ( Supplementary Fig. 1a and Supplementary Table 3). Even the largest between-phenotype F ST at Makobe is smaller than most within-phenotype F ST between islands. ...
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... and May 2005. Photos were taken of 11 (Marumbi), 241 (Luanso), 64 (Kissenda), 34 (Python) and 130 (Makobe) males in breeding dress-480 in total-immediately on capture in specially designed photographic cuvettes. Photos were scored on a 5-point (0-4) colour phenotype scale by two to five independent observers, and the mean value was used 41 ( Fig. 1). Phenotype scoring of different observers was very similar (Spearman correlations between 0.605 and 0.729, P , 0.05). Linear regressions with a quadratic term were fitted to the log-transformed counts of the colour phenotypes from each island separately using R 45 . Frequency distributions were compared between islands by ...
Citations
... Since they spend more time in deeper environments with lower temperatures and oxygen, their metabolic and growth rates decrease (Cailliet et al. 2001;Black et al. 2021). The ecological consequences of rockfishes' colourations align with expectations under environment-contingent natural selection, where colour polymorphism experiences varying degrees of fitness in response to different light environments (Gray and McKinnon 2007;Seehausen et al. 2008). ...
Body colouration, a trait under strong selection, is influenced by the visual background of the environment. The stable influence of depth on visual background dynamics is due to light attenuation along the water column. Depth is also a key factor driving diversification in Sebastes rockfishes, influencing variations in several biological traits. Comparisons between closely related species suggest that brightly coloured species (red, orange, or yellow) tend to inhabit deeper waters and have slower growth rates compared to their shallow-water counterparts with dominance of dark colours (black, brown, or grey). Here, we used 377 photos from 100 Sebastes species, along with recently developed methods of colour quantification and phylogenetic comparative analyses, to assess this trend. Our analyses confirmed the separation of body colouration regarding depth, which was accompanied by differences in growth rates and morphological traits. This indicated that variations in body colourations are included in the ongoing correlational selection process dictated by depth. Analyses of closely related species indicated that depth is an initial driver of colour differentiation and that colour differences do not progressively increase with genetic divergences. We hypothesized that the bright-coloured rockfishes are found in deeper waters because in shallow environments they are more vulnerable to the potential negative effects of UV radiation and higher predation risk, while their predation successes are lessened, in comparison to dark-coloured rockfishes. Overall, this study emphasizes the intricate relationship between genetics, environment, adaptation, and the striking diversity of body colourations observed in Sebastes rockfishes.
... The sensory environment includes environmental factors that can alter signals used during communication or how such signals are perceived. For instance, variation in light levels or spectra associated with turbidity and water depth can affect colour perception (Seehausen et al. 1997(Seehausen et al. , 2008, or the presence of chemicals in the water can alter communication with pheromones (Fisher et al. 2006, Fabian et al. 2007. ...
Animal genitalia evolve rapidly because of coevolution between male and female traits. However, how the ecological context in which mating occurs might modulate the evolution of genital traits remains poorly understood. We investigated how a change in the sensory environment (the absence of light upon cave colonization) impacted the expression of genital traits in a live-bearing fish, Poecilia mexicana (Poeciliidae), with populations in adjacent cave and surface habitats. Quantifying characteristics of the female urogenital aperture and the male gonopodium (a modified anal fin used for copulation), we found significant differences in genital traits of both sexes. Females from cave populations exhibited larger and more rounded genitalia. Males from cave populations exhibited a significantly enlarged palp, a fleshy gonopodial appendage that has been hypothesized to have sensory functions. Our results suggest that genital traits can diverge rapidly among closely related populations exposed to different environmental conditions. The absence of light could impact genital evolution directly, if some genital structures have sensory functions that compensate for the lack of visual information during copulation, or indirectly, if the absence of light impacts dynamics of sexual conflict or cryptic female choice that arise through the interaction between the sexes.
... Specifically, these systems have played a key role in understanding how divergence between close relatives is attained and maintained, highlighting the complex interplay between ecological and reproductive isolation. While some studies have highlighted ecological shifts as drivers of divergence [2][3][4][5], many others have identified sexual recognition cues as playing a central role [2,[6][7][8][9][10][11]. While the conflicting results may reflect fundamental differences between lineages, it may also be due to some signals (especially visual and auditory) being readily amenable to measurement while those that fall outside human sensory modalities are much more difficult to quantify. ...
Studies of adaptive radiations have played a central role in our understanding of reproductive isolation. Yet the focus has been on human-biased visual and auditory signals, leaving gaps in our knowledge of other modalities. To date, studies on chemical signals in adaptive radiations have focused on systems with multimodal signalling, making it difficult to isolate the role chemicals play in reproductive isolation. In this study we examine the use of chemical signals in the species recognition and adaptive radiation of Hawaiian Tetragnatha spiders by focusing on entire communities of co-occurring species, and conducting behavioural assays in conjunction with chemical analysis of their silks using gas chromatography-mass spectrometry. Male spiders significantly preferred the silk extracts of conspecific mates over those of sympatric heterospecifics. The compounds found in the silk extracts, long chain alkyl methyl ethers, were remarkably species-specific in the combination and quantity. The differences in the profile were greatest between co-occurring species and between closely related sibling species. Lastly, there were significant differences in the chemical profile between two populations of a particular species. These findings provide key insights into the role chemical signals play in the attainment and maintenance of reproductive barriers between closely related co-occurring species.
... The expression or reception of these communication signals can vary across different environments, leading to variation in RI. For instance, eutrophication and turbidity of aquatic environments caused by increased water pollution have led to hybrid swarms or hybridization among cichlids (Seehausen 1997;Seehausen et al. 2008), sticklebacks Taylor et al. 2006a;Lackey and Boughman 2013), whitefish (Vonlanthen et al. 2012;Feulner and Seehausen 2019), and swordtail fish (Banerjee et al. 2023). ...
... studied in a number of vertebrate groups (including mammals, birds, reptiles, amphibians and fishes) and in most cases, it is sexual selection for increased male size that appears to be the most important factor, with evidence for fecundity selection driven SSD evolution inconsistent or absent despite the dominance of female-biased SSD (Horne et al., 2020;Monroe et al., 2015;Seehausen et al., 2008). In the absence of vertebrate-wide comparative phylogenetic studies, this would suggest that broadly across vertebrate diversity sexual selection on male body size is stronger than fecundity selection on female body size. ...
While sexual size dimorphism (SSD) is abundant in nature, there is huge variation in both the intensity and direction of SSD. SSD results from a combination of sexual selection for large male size, fecundity selection for large female size and ecological selection for either. In most vertebrates, it is variation in the intensity of male–male competition that primarily underlies variation in SSD. In this study, we test four hypotheses regarding the adaptive value of SSD in sharks—considering the potential for each of fecundity, sexual, ecological selection and reproductive mode as the primary driver of variation in SSD between species. We also estimate past macroevolutionary shifts in SSD direction/intensity through shark phylogeny. We were unable to find evidence of significant SSD in early sharks and hypothesise that SSD is a derived state in this clade, that has evolved independently of SSD observed in other vertebrates. Moreover, there is no significant relationship between SSD and fecundity, testes mass or oceanic depth in sharks. However, there is evidence to support previous speculation that reproductive mode is an important determinant of interspecific variation in SSD in sharks. This is significant as in most vertebrates sexual selection is thought to be the primary driver of SSD trends, with evidence for the role of fecundity selection in other clades being inconsistent at best. While the phylogenetic distribution of SSD among sharks is superficially similar to that observed in other vertebrate clades, the relative importance of selective pressures underlying its evolution appears to differ.
... Assortative mating incompatibility describes incompatibility between the gene(s) underlying a given phenotypic mating trait and the gene(s) underlying the preference for that trait (see Merrill et al. 2023). These can evolve via the Fisherian runaway process of sexual selection, such as in morphologically and ecologically similar species of Laupala crickets (Xu and Shaw 2019), or via environment-dependent sensory drive selection, such as in ecologically divergent species of cichlid fishes (Seehausen et al. 2008b). Incompatibilities resulting from these different selective regimes may also differ in how they are expected to decrease fitness in consecutive generations of hybrids (Lindtke and Buerkle 2015). ...
... While strictly intrinsic incompatibilities can only manifest as postmating barriers, behavioral and ecological incompatibilities can act as both premating barriers (McKinnon et al. 2004), and as postmating barriers that reduce the reproductive fitness of hybrids (Gottsberger and Mayer 2007;Arnegard et al. 2014;Bay et al. 2017). The observation that alleles underlying behavioral (Seehausen et al. 2008b;Meier et al. 2017a), ecological (Lamichhaney et al. 2015;Martinez Barrio et al. 2016), and environment-independent intrinsic (Sicard et al. 2015;Fuller et al. 2018) incompatibilities can be older than the split between sister taxa suggest that all these types of incompatibilities may be present before the onset of speciation and may be segregating already in the ancestral population. (Xie et al. 2007;Roberts Kingman et al. 2021). ...
Hybridization, or interbreeding between different taxa, was traditionally considered to be rare and to have a largely detrimental impact on biodiversity, sometimes leading to the breakdown of reproductive isolation and even to the reversal of speciation. However, modern genomic and analytical methods have shown that hybridization is common in some of the most diverse clades across the tree of life, sometimes leading to rapid increase of phenotypic variability, to introgression of adaptive alleles, to the formation of hybrid species, and even to entire species radiations. In this review, we identify consensus among diverse research programs to show how the field has progressed. Hybridization is a multifaceted evolutionary process that can strongly influence species formation and facilitate adaptation and persistence of species in a rapidly changing world. Progress on testing this hypothesis will require cooperation among different subdisciplines.
... Comunicación acústica, Comunicación animal, Variación geográfica intraespecífica otros tipos de canto (e.g., canto de cortejo, canto de auxilio). La variación geográfica intraespecífica en señales de comunicación podría influir directamente en procesos de reconocimiento de especies, selección de pareja y flujo genético entre poblaciones; por lo tanto, es importante documentar características de señales de comunicación en varias poblaciones de una misma especie (Irwin et al., 2001;Boughman, 2002;Seehausen et al., 2008;Wilkins et al., 2013). ...
La comunicación acústica es la modalidad de comunicación más estudiada en anuros. No obstante, del repertorio de señales acústicas que se conoce para anuros, tradicionalmente se ha descrito el canto de anuncio, mientras que cantos de cortejo y
de auxilio son menos conocidos. Dado que caracterizar las señales acústicas en anuros es útil para estudios de ecología, sistemática y evolución, y en la implementación de estrategias de manejo y conservación, en este estudio describimos tres tipos de canto en la rana de cristal Hyalinobatrachium tatayoi (Centrolenidae). Entre julio y diciembre de 2022 realizamos 21 salidas de campo nocturnas a una localidad en la vertiente occidental de la cordillera Central, en el departamento del Quindío, Colombia. Obtuvimos grabaciones de 407 cantos de anuncio emitidos por 21 machos, 230 cantos de cortejo emitidos por nueve machos, y ocho cantos de auxilio, dos emitidos por un macho y seis por una hembra. Nuestra descripción del canto de anuncio y cortejo, basada en 13 parámetros (siete espectrales, seis temporales), es la más detallada de las publicadas hasta la fecha para H. tatayoi. Además, proviene de una población que se encuentra separada de otras poblaciones para las cuales se han descrito estos cantos, por la presencia de dos cordilleras. Una comparación preliminar del canto de anuncio y de cortejo entre poblaciones de H. tatayoi permite visualizar poca variación geográfica intraespecífica en la frecuencia dominante y la duración del canto. Hasta la fecha, se conocen cuatro tipos de canto del repertorio de señales acústicas en H. tatayoi: canto de anuncio, canto de cortejo, canto de auxilio, y canto agonístico. Aunque no todos los parámetros de estos tipos de canto han sido cuantificados con el mismo nivel de detalle, H. tatayoi se convierte en una de las especies de Centrolenidae en que mejor se conoce su repertorio de señales acústicas.
... Third, larger areas allow for more opportunity for allopatric, parapatric, and sympatric speciation (Coyne & Price, 2000;Gavrilets & Vose, 2005). Fourth, intermediate zones of selective pressure are more frequent in larger areas, and these zones are more conducive for speciation (i.e., selection gradient effect; Doebeli & Dieckmann, 2003;Kawata et al., 2007;Seehausen et al., 2008). The aforementioned factors are possible explanations as to why the largest, the most geologically complex, and the transition zone islands and/or archipelagoes of the IAA are the centers of diversity for Cyrtandra and harbor the widest morphological range for the genus (see graphical abstract; Burtt, 2001;Atkins et al., 2013;Clark et al., 2013;Atkins & Kartonegro, 2021;Olivar et al., 2022;Bramley et al., 2023). ...
The general dynamic model (GDM) of oceanic island biogeography views oceanic islands predominantly as sinks rather than sources of dispersing lineages. To test this, we conducted a biogeographic analysis of a highly successful insular plant taxon, Cyrtandra , and inferred the directionality of dispersal and founder events throughout the four biogeographical units of the Indo‐Australian Archipelago (IAA), namely Sunda, Wallacea, Philippines, and Sahul. Sunda was recovered as the major source area, followed by Wallacea, a system of oceanic islands. The relatively high number of events originating from Wallacea is attributed to its central location in the IAA and its complex geological history selecting for increased dispersibility. We also tested if diversification dynamics in Cyrtandra follow predictions of adaptive radiation, which is the dominant process as per the GDM. Diversification dynamics of dispersing lineages of Cyrtandra in the Southeast Asian grade showed early bursts followed by a plateau, which is consistent with adaptive radiation. We did not detect signals of diversity‐dependent diversification, and this is attributed to Southeast Asian cyrtandras occupying various niche spaces, evident by their wide morphological range in habit and floral characters. The Pacific clade, which arrived at the immaturity phase of the Pacific Islands, showed diversification dynamics predicted by the island immaturity speciation pulse model (IISP), wherein rates increase exponentially, and their morphological range is controlled by the least action effect favoring woodiness and fleshy fruits. Our study provides a first step toward a framework for investigating diversification dynamics as predicted by the GDM in highly successful insular taxa.
... The proliferation of forms characterising adaptive radiations is often accompanied by modifications to sensory systems [1][2][3][4], and there is considerable evidence for selection on sensory systems within the context of rapid speciation events [5]. In principle, during ecological speciation, selection will tune sensory systems to the specific requirements of organisms' respective niches, affecting both function and morphology [6]. ...
... In principle, during ecological speciation, selection will tune sensory systems to the specific requirements of organisms' respective niches, affecting both function and morphology [6]. Thus, to investigate the speciation process we require an understanding of how organisms' sensory systems adapt to maximise fitness within their local environments [2]. ...
... Research on the evolution of sensory systems in fish has largely focused on vision, and this has clearly demonstrated that visual adaptation is important for both initial divergence and the maintenance of reproductive isolation in sympatry [1,2,4]. However, the ability of fishes to survive and adapt to their environment is also dependent on the detection of water flow through the mechanoreceptive lateral line system [9,11,12]. ...
Background
The mechanosensory lateral line system is an important sensory modality in fishes, informing multiple behaviours related to survival including finding food and navigating in dark environments. Given its ecological importance, we may expect lateral line morphology to be under disruptive selection early in the ecological speciation process. Here we quantify the lateral line system morphology of two ecomorphs of the cichlid fish Astatotilapia calliptera in crater Lake Masoko that have diverged from common ancestry within the past 1,000 years.
Results
Based on geometric morphometric analyses of CT scans, we show that the zooplanktivorous benthic ecomorph that dominates the deeper waters of the lake has large cranial lateral line canal pores, relative to those of the nearshore invertebrate-feeding littoral ecomorph found in the shallower waters. In contrast, fluorescence imaging revealed no evidence for divergence between ecomorphs in the number of either superficial or canal neuromasts. We illustrate the magnitude of the variation we observe in Lake Masoko A. calliptera in the context of the neighbouring Lake Malawi mega-radiation that comprises over 700 species.
Conclusions
These results provide the first evidence of divergence in this often-overlooked sensory modality in the early stages of ecological speciation, suggesting that it may have a role in the broader adaptive radiation process.
... This can lead to difficulty choosing an appropriate mate if interspecific nuptial color differences are masked (e.g. Pundamilia pundamilia and P. nyererei; Seehausen et al., 2008) or difficulty distinguishing high quality mates (e.g., threespine sticklebacks, Gasterosteus aculeatus; Candolin et al., 2015). There is strong evidence for altered behavior in response to rapidly changing sensory landscapes across a wide array of taxa (Candolin and Wong, 2019), with consequences at the interspecific level and within species. ...
... et al., 2016b;Reid et al., 2019;Ricciardi and Rasmussen, 1999), and resulting environmental changes from turbidity may also influence a number of visually-guided behaviors including interspecific (e.g., predator-prey relationships; Abrahams and Kattenfeld, 1997;Utne-Palm, 2002) and intraspecific (e.g., reproductive behavior; Candolin, et al., 2015;Seehausen et al,. 2008) interactions. Such behavioral shifts can lead to decreased foraging efficiency (Nieman and Gray, 2019) and ...
... potentially disrupt species barriers (Seehausen et al., 2008;van der Sluijs et al., 2011). Reduction in the amount of light and change in spectral composition associated with turbidity could alter investment in vision (e.g., via larger eyes and optic lobes to maintain visual detection thresholds (Dugas and Franssen, 2012;Huber and Rylander, 1992;Huber et al., 1997)). ...
Natural variation in environmental turbidity correlates with variation in the visual sensory system of many fishes, suggesting that turbidity may act as a strong selective agent on visual systems. Since many aquatic systems experience increased turbidity due to anthropogenic perturbations, it is important to understand the degree to which fish can respond to rapid shifts in their visual environment, and whether such responses can occur within the lifetime of an individual. We examined whether developmental exposure to turbidity (Clear <5 NTU, Turbid ∼9 NTU) influenced the size of morphological structures associated with vision in the African cichlid Pseudocrenilabrus multicolor. Parental fish were collected from two sites (clear swamp, turbid river) in western Uganda. F1 broods from each population were split and reared under clear and turbid rearing treatments until maturity. We measured morphological traits associated with the visual sensory system (eye diameter, pupil diameter, axial length, brain mass, optic tectum volume) over the course of development. Age was significant in explaining variation in visual traits even when standardized for body size, suggesting an ontogenetic shift in the relative size of eyes and brains. When age groups were analyzed separately, young fish reared in turbid water grew larger eyes than fish reared in clear conditions. Population was important in the older age category, with swamp-origin fish having relatively larger eyes and optic lobes relative to river-origin fish. Plastic responses during development may be important in responding to a more variable visual environment associated with anthropogenically induced turbidity.
