Topi K. Lehtonen

Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes

The polychromatic and trophically polymorphic Midas cichlid fish species complex (Amphilophus cf. citrinellus) is an excellent model system for studying the mechanisms of speciation and patterns of phenotypic diversification in allopatry and in sympatry. Here, we first review research to date on the species complex and the geological history of its habitat. We analyse body shape variation from all currently described species in the complex, sampled from six crater lakes (maximally 1.2–23.9 kyr old) and both great lakes in Nicaragua. We find that Midas cichlid populations in each lake have their own characteristic body shape. In lakes with multiple sympatric species of Midas cichlid, each species has a distinct body shape. Across the species complex, most body shape change relates to body depth, head, snout and mouth shape and caudal peduncle length. There is independent parallel evolution of an elongate limnetic species in at least two crater lakes. Mitochondrial genetic diversity is higher in crater lakes with multiple species. Midas cichlid species richness increases with the size and age of the crater lakes, though no such relationship exists for the other syntopic fishes. We suggest that crater lake Midas cichlids follow the predicted pattern of an adaptive radiation, with early divergence of each crater lake colonization, followed by intralacustrine diversification and speciation by ecological adaptation and sexual selection.

Color Assortative Mating Contributes to Sympatric Divergence of Neotropical Cichlid Fish

It is still debated vigorously whether sexual selection can result in speciation without physical barriers to gene flow. In this study, we used field data and molecular methods to investigate the gold-normal color polymorphism in two endemic cichlid fish species of crater lake Xiloá, Nicaragua. We found significant assortative mating by color in both Amphilophus xiloaensis and A. sagittae. Focusing on A. xiloaensis, microsatellite allele frequencies, an assignment test, and model-based cluster analysis demonstrates significant and clear genetic differentiation (F ST = 0.03) between gold and normal individuals in sympatry. In addition, we find genetic differentiation between all three sympatric and ecologically distinct Midas cichlid species of Lake Xiloá, A. amarillo, A. sagittae, and A. xiloaensis (F ST = 0.03 – 0.19), and clear genetic isolation of these species from their closest relative (A. citrinellus) in the neighboring great lake Managua. The A. xiloaensis gold morph is genetically more distinct from the lakes other two Midas cichlid species than is A. xiloaensis-normal. Thus, we have identified sexual isolation based on color that is evident in population genetics and mate choice. Our results suggest that sexual selection through color assortative mating may play an important role in incipient sympatric speciation in Midas cichlids of Nicaragua.

Repeatability of mating preferences in the sand goby

Variation among individuals in mate choice has important implications for the evolution of sexually selected traits. For example, it offers an explanation for the continued existence of heritable genetic variation in sexually selected male traits. In this study, we first tested the suitability of association tests for assessing female mate preferences in the sand goby, Pomatoschistus minutus. Sand goby females showed sexually motivated association preferences that were repeatable and corresponded to actual mating decisions. We then compared the correlation between the preferences of two different females presented to the same male pair with the correlation between preferences of single females tested twice. We found a weak correlation between preferences in the two-female treatment, while the correspondence between preferences was much higher for the single-female treatment. These results are in accordance with the possibility that sand goby females show genetically based, individual differences in mate preferences.

Fluctuating mate preferences in a marine fish.

According to theory, directional female choice for male sexual ornaments is expected to erode underlying genetic variation. Considerable attention, in this regard, has been given to understanding the ubiquity of heritable genetic variation in both female choice and male sexual traits. One intriguing possibility emerging from this work is that persistent genetic variation could be maintained, over time, by variation in female mate preferences. Here, we report the results of a four-year study showing significant year-to-year fluctuations in mate preferences in a small marine fish, the sand goby, Pomatoschistus minutus. Although the average size of mature fish varied across years, we were unable to find direct evidence linking this variation to differences in female preferences among years. Our results, nevertheless, underscore the importance of temporal fluctuations in female mate preferences, as these can have important consequences for understanding variation in sexual traits and the intensity of sexual selection.

A high aggression strategy for smaller males

Male-male conflict is common among animals, but questions remain as to when, how and by whom aggression should be initiated. Factors that affect agonistic strategies include residency, the value of the contested resource and the fighting ability of the two contestants. We quantified initiation of aggression in a fish, the desert goby, Chlamydogobius eremius, by exposing nest-holding males to a male intruder. The perceived value of the resource (the nest) was manipulated by exposing half of the residents to sexually receptive females for two days before the trial. Resident male aggression, however, was unaffected by perceived mating opportunities. It was also unaffected by the absolute and relative size of the intruder. Instead resident aggression was negatively related to resident male size. In particular, smaller residents attacked sooner and with greater intensity compared to larger residents. These results suggest that resident desert goby males used set, rather than conditional, strategies for initiating aggression. If intruders are more likely to flee than retaliate, small males may benefit from attacking intruders before these have had an opportunity to assess the resident and/or the resource.

The interval between sexual encounters affects male courtship tactics in a desert-dwelling fish

Courtship displays are often important in determining male mating success but can also be costly. Thus, instead of courting females indiscriminately, males might be expected to adjust their signalling effort strategically. Theory, however, predicts that such adjustments should depend on the rate with which males encounter females, a prediction that has been subject to very little empirical testing. Here, we investigate the effects of female encounter rate on male courtship intensity by manipulating the time interval between sequential presentations of large (high quality) and small (low quality) females in a fish, the Australian desert goby Chlamydogobius eremius. Males that were presented with a small female immediately after a large female reduced their courtship intensity significantly. However, males courted large and small females with equal intensity if the interval between the sequential presentations was longer. Our results suggest that mate encounter rate is an important factor shaping male reproductive decisions and, consequently, the evolutionary potential of sexual selection.

Territorial aggression can be sensitive to the status of heterospecific intruders.

Territorial animals are known to be able to differentiate between intruding individuals posing a low or high threat and adjust their aggressive response accordingly. However, plastic territorial aggression based on recognising individuals with different attributes is typically assumed to be relevant only in the context of conspecific interactions. In this study, we investigated territorial aggression of neotropical cichlid fish in their natural habitat to assess whether responses to different types of individuals of another species can also be plastic. We show that arrow cichlids (Amphilophus zaliosus) adjusted their territorial aggression regarding the status of heterospecific intruders: breeding individuals of Amphilophus astorquii received a lower level of aggression than non-breeders. The same pattern was also found for the two different types of A. astorquii individuals intruding into conspecific territories. These results suggest that heterospecific individuals should not be ignored when considering selection pressures shaping plasticity of aggressive behaviour in territorial animals.

Colour biases in territorial aggression in a Neotropical cichlid fish

Discrete colour morphs have provided important insights into the evolution of phenotypic diversity. One of the mechanisms that can help to explain coexistence of ecologically similar colour morphs and incipient species is (colour) biased aggression, which has the potential to promote continued existence of the morphs in a frequency-dependent manner. I addressed colour biases in territorial aggression in a field-based study on a Neotropical cichlid fish species, Amphilophus sagittae, which has two ecologically indistinguishable colour morphs that mate assortatively. I found that A. sagittae, in particular females, were more aggressive towards models of their own colour than those mimicking colours of the other morph. Such a behavioural pattern should result in a selection regime that benefits the rarer morph, and hence could help explain how novel, rare phenotypes may avoid competitive exclusion.

Crater lake colonization by neotropical cichlid fishes

Volcanic crater lakes are isolated habitats that are particularly well suited to investigating ecological and evolutionary divergence and modes of speciation. However, the mode, frequency, and timing of colonization of crater lakes have been difficult to determine. We used a statistical comparative phylogeographic approach, based on a mitochondrialDNA dataset, to infer the colonization history of two Nicaraguan crater lakes by populations of genetically and ecologically divergent cichlid lineages: Midas (Amphilophus cf. citrinellus complex) and moga (Hypsophrys nematopus). We compared estimates of diversity among populations within the two cichlid lineages and found that Midas were the most genetically diverse. From an approximate Bayesian computation analysis, we inferred that the crater lakes were each founded by both cichlid lineages in single waves of colonization: Masaya 5800 ± 300 years ago and Xiloá 5400 ± 750 years ago. We conclude that natural events are likely to have a dominant role in colonization of the crater lakes. Further, our findings suggest that the higher species richness and more rapid evolution of the Midas species complex, relative to other lineages of fishes in the same crater lakes, cannot be explained by earlier or more numerous colonization events.

Adjustment of brood care behaviour in the absence of a mate in two species of Nicaraguan crater lake cichlids

In many taxa, parental strategies can vary among individuals. This is especially true in species with biparental care, with males, more often than females, deserting their mates. While there is an abundance of theoretical predictions and empirical data on factors inducing mate abandonment by males, much less is known about what consequences this may have on female behaviour, particularly in the field and in non-avian systems. Here, we compared brood defence rate, behavioural defence types, and brood success of solitary and paired females in two species of Neotropical cichlid fish in their natural habitat. In terms of the rate of territorial aggression towards potential brood predators, solitary females were able to fully compensate in the absence of a male but, in so doing, ended up maintaining smaller territories, which appeared to compromise offspring fitness in at least one of the two species. Hence, our results suggest that even extensive quantitative compensation in parental effort by solitary females may not be enough to ensure adequate qualitative compensation for the lack of male participation, highlighting the importance of distinguishing between these two aspects of compensatory parental care.