Cleaner fish recognize self in a mirror via self-face recognition like humans.

Some animals have the remarkable capacity for mirror self-recognition (MSR), yet any implications for self-awareness remain uncertain and controversial. This is largely because explicit tests of the two potential mechanisms underlying MSR are still lacking: mental image of the self and kinesthetic visual matching. Here, we test the hypothesis that MSR ability in cleaner fish, Labroides dimidiatus, is associated with a mental image of the self, in particular the self-face, like in humans. Mirror-naive fish initially attacked photograph models of both themselves and unfamiliar strangers. In contrast, after all fish had passed the mirror mark test, fish did not attack their own (motionless) images, but still frequently attacked those of unfamiliar individuals. When fish were exposed to composite photographs, the self-face/unfamiliar body were not attacked, but photographs of unfamiliar face/self-body were attacked, demonstrating that cleaner fish with MSR capacity recognize their own facial characteristics in photographs. Additionally, when presented with self-photographs with a mark placed on the throat, unmarked mirror-experienced cleaner fish demonstrated throat-scraping behaviors. When combined, our results provide clear evidence that cleaner fish recognize themselves in photographs and that the likely mechanism for MSR is associated with a mental image of the self-face, not a kinesthetic visual-matching model. Humans are also capable of having a mental image of the self-face, which is considered an example of private self-awareness. We demonstrate that combining mirror test experiments with photographs has enormous potential to further our understanding of the evolution of cognitive processes and private self-awareness across nonhuman animals.

Male Guppies Recognize Familiar Conspecific Males by Their Face.

Individual recognition is a necessary cognitive ability for the maintenance of stable social relationships. Recent studies have shown that like primates, some fish species can distinguish familiar fish from unfamiliar strangers via face-recognition. However, the taxa of the studied fish species are restricted (within Perciformes) and the visual signal used for the recognition of fish remains unclear. Here, we investigated the visual signal for individual-recognition in males of a sexually dichromatic guppy (Poecilia reticulata, Cyprinodontiformes). Using guppy males, we examined the hypothesis that fish distinguish between familiar individuals and unknown strangers by their faces rather than by body coloration. We randomly presented focal fish with four types of composite photo-models: familiar (familiar-face and familiar-body = F/F), stranger (stranger-face and stranger-body = S/S), familiar face combined with stranger body (F/S) and stranger face combined with familiar body (S/F). Focal males infrequently attacked familiar-face models but frequently attacked stranger-face models, regardless of body types. These behavioral reactions indicate that guppy males discriminate between familiar and stranger males by their face, not body coloration with wide variation. Importantly, male faces contain clear individual-variation in white/metallic colored patches on the operculum visible for humans. Considering the photo-model, our results suggest that these patches might be an important visual stimulus for face-recognition in guppy males, like some cichlids. Comparative examination among males of different guppy variants, including wild type phenotype, suggests that the face color-patch is stable regardless of variation in body color, with a different genetic mechanism potentially underlying face and body colors.

Pervasive admixture and the spread of a large-lipped form in a cichlid fish radiation.

Adaptive radiations have proven important for understanding the mechanisms and processes underlying biological diversity. The convergence of form and function, as well as admixture and adaptive introgression, are common in adaptive radiations. However, distinguishing between these two scenarios remains a challenge for evolutionary research. The Midas cichlid species complex (Amphilophus spp.) is a prime example of adaptive radiation, with phenotypic diversification occurring at various stages of genetic differentiation. One species, A. labiatus, has large fleshy lips, is associated with rocky lake substrates, and occurs patchily within Lakes Nicaragua and Managua. By contrast, the similar, but thin-lipped, congener, A. citrinellus, is more common and widespread. We investigated the evolutionary history of the large-lipped form, specifically regarding whether the trait has evolved independently in both lakes from ancestral thin-lipped populations, or via dispersal and/or admixture events. We collected samples from distinct locations in both lakes, and assessed differences in morphology and ecology. Using RAD-seq, we genotyped thousands of SNPs to measure population structure and divergence, demographic history, and admixture. We found significant between-species differences in ecology and morphology, local intraspecific differences in body shape and trophic traits, but only limited intraspecific variation in lip shape. Despite clear ecological differences, our genomic approach uncovered pervasive admixture between the species and low genomic differentiation, with species within lakes being genetically more similar than species between lakes. Taken together, our results suggest a single origin of large-lips, followed by pervasive admixture and adaptive introgression, with morphology being driven by local ecological opportunities, despite ongoing gene-flow.

Las radiaciones adaptativas han demostrado ser clave para entender los mecanismos y procesos responsables de la diversidad biológica. La convergencia en forma y función, así como la mezcla genética y la introgresión adaptativa, son algo común en las radiaciones adaptativas. Sin embargo, distinguir entre estos dos escenarios sigue siendo un desafío para la biología evolutiva. El complejo de especies del cíclido de Midas (Amphilophus spp.) es un ejemplo paradigmático de radiación adaptativa, con diversidad fenotípica en varias etapas de diferenciación genética. Una de las especies, A. labiatus, que tiene labios grandes y carnosos, se asocia a zonas rocosas de los lagos, y tiene una distribución irregular en los lagos Nicaragua y Managua. En cambio, A. citrinellus, es una especie similar pero con labios finos, más común y con una distribución más amplia. Investigamos la historia evolutiva de la especie de labios grandes y, en concreto, si este rasgo ha evolucionado de forma independiente en los dos grandes lagos nicaragüenses a partir de poblaciones ancestrales de labios finos, o si por el contrario se ha dispersado mediante migración y/o mezcla genética. Colectamos muestras de distintas localidades en ambos lagos y evaluamos las diferencias en morfología y ecología. Genotipamos miles de SNPs utilizando RAD-seq para medir la estructura genética, la divergencia, la historia demográfica y la mezcla genética de las poblaciones. Encontramos diferencias significativas entre especies en ecología y morfología, diferencias intraespecíficas locales en la forma del cuerpo y rasgos tróficos, pero sólo una limitada variación intraespecífica en la forma de los labios. A pesar de las claras diferencias ecológicas, el análisis genómico desveló una intensa mezcla genética entre especies, y una limitada diferenciación genómica, encontrando mayor semejanza genética entre especies dentro de un mismo lago, que entre especies de distintos lagos. Nuestros resultados sugieren un origen único de la especie de labios gruesos seguido de mezcla genética e introgresión adaptativa, e indican que la morfología habría sido modelada por las oportunidades ecológicas locales, a pesar del flujo génico.

Parental effects influence life history traits and covary with an environmental cline in common frog populations.

Across latitudinal clines, the juvenile developmental rates of ectotherms often covary with the length of the growing season, due to life-history trade-offs imposed by the time-constrained environments. However, as the start of the growing season often varies substantially across years, adaptive parental effects on juvenile developmental rates may mediate the costs of a delayed season. By employing a meta-analysis, we tested whether larval developmental rates across a latitudinal cline of the common frog (Rana temporaria) are affected by fluctuating onsets of breeding, across years. We predicted that larval developmental rate will be inversely related to the onset of breeding, and that northern populations will be more prone to shorten their developmental rate in response to late breeding, as the costs of delayed metamorphosis should be highest in areas with a shorter growing season. We found that the larval period of both northern and southern populations responded to parental environmental conditions to a similar degree in absolute terms, but in different directions. In northern populations, a late season start correlated with decreased development time, suggesting that the evolution of parental effects aids population persistence in time-constrained environments. In southern populations, late season start correlated with increased development time, which could potentially be explained as a predator avoidance strategy. Our findings suggest that local ecological variables can induce adaptive parental effects, but responses are complex, and likely trade-off with other ecological factors.

Allopatry, competitor recognition and heterospecific aggression in crater lake cichlids.

BACKGROUND: Aggressive behaviour can have significant evolutionary consequences-not only within species, but also in the context of heterospecific interactions. Here, we carried out an experimental field study to investigate the importance of phenotypic similarity on levels of aggression between species whilst controlling for familiarity effects using manipulated allopatric stimuli. Specifically, we investigated aggressive responses of territory holding males and females in two species of Neotropical cichlid fish, Amphilophus sagittae and Hypsophrys nicaraguensis, that differ in their phenotypic similarity to our allopatric stimulus species, Amphilophus astorquii. RESULTS: We found that, independent of phenotypic similarity (and correlated phylogenetic proximity) between the territory holders and intruder, territorial aggression was not adjusted in relation to allopatric intruder colour markings that are associated with different levels of threat and known to provoke different responses in a sympatric setting. We also found that males and females did not differ in their overall patterns of aggression adjustment towards intruder cues. Nevertheless, the two focal species, which share the same breeding grounds and external threats, exhibited different sex roles in breeding territory defence. CONCLUSION: Together with earlier studies assessing hetrospecific aggression in sympatry, our current results highlight the importance of coevolution and learning in species interactions.

Cichlid Fish Use Coloration as a Cue to Assess the Threat Status of Heterospecific Intruders.

The ability to assess the threat posed by competitors, and to respond appropriately, is important for reducing the costs of aggression. In this respect, aggression directed toward heterospecifics is often just as significant as aggression among conspecifics. This is especially true for cichlid fish that share breeding grounds with heterospecifics. Indeed, cichlids are known to differentiate not only between conspecifics that pose different levels of threat but also between heterospecific territorial intruders by directing more aggression toward nonbreeding individuals. To assess whether the ability to make such distinctions could be based on color cues alone, we carried out a field study in which we experimentally presented Amphilophus sagittae cichlid pairs with model intruders of a sympatric congener, Amphilophus xiloaensis, in breeding versus nonbreeding coloration. Consistent with our prediction, we found that A. sagittae exhibited more aggression toward A. xiloaensis models of the latter color type. The results are, to our knowledge, the first to show that territory holders can, based on coloration alone, assess variation among individuals of a species other than their own in the threat posed to offspring survival.

Heterospecific aggression bias towards a rarer colour morph.

Colour polymorphisms are a striking example of phenotypic diversity, yet the sources of selection that allow different morphs to persist within populations remain poorly understood. In particular, despite the importance of aggression in mediating social dominance, few studies have considered how heterospecific aggression might contribute to the maintenance or divergence of different colour morphs. To redress this gap, we carried out a field-based study in a Nicaraguan crater lake to investigate patterns of heterospecific aggression directed by the cichlid fish, Hypsophrys nicaraguensis, towards colour polymorphic cichlids in the genus Amphilophus. We found that H. nicaraguensis was the most frequent territorial neighbour of the colour polymorphic A. sagittae. Furthermore, when manipulating territorial intrusions using models, H. nicaraguensis were more aggressive towards the gold than dark colour morph of the sympatric Amphilophus species, including A. sagittae. Such a pattern of heterospecific aggression should be costly to the gold colour morph, potentially accounting for its lower than expected frequency and, more generally, highlighting the importance of considering heterospecific aggression in the context of morph frequencies and coexistence in the wild.

The relative effects of pace of life-history and habitat characteristics on the evolution of sexual ornaments: A comparative assessment.

Selection may favor greater investment into sexual ornaments when opportunities for future reproduction are limited, for example, under high adult mortality. However, predation, a key driver of mortality, typically selects against elaborate sexual ornaments. Here, we examine the evolution of sexual ornaments in killifishes, which have marked contrasts in life-history strategy among species and inhabit environments that differ in accessibility to aquatic predators. We first assessed if the size of sexual ornaments (unpaired fins) influenced swimming performance. Second, we investigated whether the evolution of larger ornamental fins is driven primarily by the pace of life-history (investment into current vs. future reproduction) or habitat type (a proxy for predation risk). We found that larger fins negatively affected swimming performance. Further, males from species inhabiting ephemeral habitats, with lower predation risk, had larger fins and greater sexual dimorphism in fin size, compared to males from more accessible permanent habitats. We show that enlarged ornamental fins, which impair locomotion, evolve more frequently in environments that are less accessible to predators, without clear associations to life-history strategy. Our results provide a rare link between the evolution of sexual ornaments, effects on locomotion performance, and natural selection on ornament size potentially through habitat differences in predation risk.

Variation in developmental rates is not linked to environmental unpredictability in annual killifishes.

Comparative evidence suggests that adaptive plasticity may evolve as a response to predictable environmental variation. However, less attention has been placed on unpredictable environmental variation, which is considered to affect evolutionary trajectories by increasing phenotypic variation (or bet hedging). Here, we examine the occurrence of bet hedging in egg developmental rates in seven species of annual killifish that originate from a gradient of variation in precipitation rates, under three treatment incubation temperatures (21, 23, and 25°C). In the wild, these species survive regular and seasonal habitat desiccation, as dormant eggs buried in the soil. At the onset of the rainy season, embryos must be sufficiently developed in order to hatch and complete their life cycle. We found substantial differences among species in both the mean and variation of egg development rates, as well as species-specific plastic responses to incubation temperature. Yet, there was no clear relationship between variation in egg development time and variation in precipitation rate (environmental predictability). The exact cause of these differences therefore remains enigmatic, possibly depending on differences in other natural environmental conditions in addition to precipitation predictability. Hence, if species-specific variances are adaptive, the relationship between development and variation in precipitation is complex and does not diverge in accordance with simple linear relationships.

Fast life-histories are associated with larger brain size in killifishes.

The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands.

Macroevolutionary evidence suggests trait-dependent coevolution between behavior and life-history.

Species with fast life-histories typically prioritize current over future reproductive events, compared to species with slow life-histories. These species therefore require greater energetic input into reproduction, and also likely have less time to realize their reproductive potential. Hence, behaviors that increase access to both resources and mating opportunities, at a cost of increased mortality risk, could coevolve with the pace of life-history. However, whether this prediction holds across species, remains untested under standardized conditions. Here, we test how risky behaviors, which facilitate access to resources and mating opportunities (i.e., activity, boldness, and aggression), along with metabolic rate, coevolve with the pace of life-history across 20 species of killifish that present remarkable divergences in the pace of life-history. We found a positive association between the pace of life-history and aggression, but interestingly not with other behavioral traits or metabolic rate. Aggression is linked to interference competition, and in killifishes is often employed to secure mates, while activity and boldness are more relevant for exploiting energetic resources. Our results suggest that the trade-off between current and future reproduction plays a more prominent role in shaping mating behavior, while behaviors related to energy acquisition may be influenced by ecological factors.

Time-limited environments affect the evolution of egg-body size allometry.

Initial offspring size is a fundamental component of absolute growth rate, where large offspring will reach a given adult body size faster than smaller offspring. Yet, our knowledge regarding the coevolution between offspring and adult size is limited. In time-constrained environments, organisms need to reproduce at a high rate and reach a reproductive size quickly. To rapidly attain a large adult body size, we hypothesize that, in seasonal habitats, large species are bound to having a large initial size, and consequently, the evolution of egg size will be tightly matched to that of body size, compared to less time-limited systems. We tested this hypothesis in killifishes, and found a significantly steeper allometric relationship between egg and body sizes in annual, compared to nonannual species. We also found higher rates of evolution of egg and body size in annual compared to nonannual species. Our results suggest that time-constrained environments impose strong selection on rapidly reaching a species-specific body size, and reproduce at a high rate, which in turn imposes constraints on the evolution of egg sizes. In combination, these distinct selection pressures result in different relationships between egg and body size among species in time-constrained versus permanent habitats.