Rüdiger Riesch

Stability and group specificity of stereotyped whistles in resident killer whales, Orcinus orca, off British Columbia

Resident killer whales off British Columbia form four acoustically distinct clans, each with a unique dialect of discrete pulsed calls. Three clans belong to the northern and one to the southern community. Resident killer whales also produce tonal whistles, which play an important role in close-range communication within the northern community. However, there has been no comparative analysis of repertoires of whistles across clans. We investigated the structural characteristics, stability and group specificity of whistles in resident killer whales off British Columbia. Acoustic recordings and behavioural observations were made between 1978 and 2003. Whistles were classified spectrographically and additional observers were used to confirm our classification. Whistles were compared across clans using discriminant function analysis. We found 11 types of stereotyped whistles in the northern and four in the southern community with some of the whistle types being stable over at least 13 years. In northern residents, 10 of the 11 whistle types were structurally identical in two of the three acoustic clans, whereas the whistle types of southern residents differed clearly from those of the northern residents. Our study shows that killer whales that have no overlap in their call repertoire use essentially the same set of stereotyped whistles. Shared stereotyped whistles might provide a community-level means of recognition that facilitates association and affiliation of members of different clans, which otherwise use distinct signals. We further suggest that vocal learning between groups plays an important role in the transmission of whistle types.

Toxic hydrogen sulfide and dark caves: life‐history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae)

Life-history traits are very sensitive to extreme environmental conditions, because resources that need to be invested in somatic maintenance cannot be invested in reproduction. Here we examined female life-history traits in the Mexican livebearing fish Poecilia mexicana from a variety of benign surface habitats, a creek with naturally occurring toxic hydrogen sulfide (H2S), a sulfidic cave, and a non-sulfidic cave. Previous studies revealed pronounced genetic and morphological divergence over very small geographic scales in this system despite the absence of physical barriers, suggesting that local adaptation to different combinations of two selection factors, toxicity (H2S) and darkness, is accompanied by very low rates of gene flow. Hence, we investigated life-history divergence between these populations in response to the selective pressures of darkness and/or toxicity. Our main results show that toxicity and darkness both select for (or impose constraints on) the same female trait dynamics: reduced fecundity and increased offspring size. Since reduced fecundity in the sulfur cave population was previously shown to be heritable, we discuss how divergent life-history evolution may promote further ecological divergence: for example, reduced fecundity and increased offspring autonomy are clearly beneficial in extreme environments, but fish with these traits are outcompeted in benign habitats.

Survival in an extreme habitat: the roles of behaviour and energy limitation

Extreme habitats challenge animals with highly adverse conditions, like extreme temperatures or toxic substances. In this paper, we report of a fish (Poecilia mexicana) inhabiting a limestone cave in Mexico. Several springs inside the cave are rich in toxic H2S. We demonstrate that a behavioural adaptation, aquatic surface respiration (ASR), allows for the survival of P. mexicana in this extreme, sulphidic habitat. Without the possibility to perform ASR, the survival rate of P. mexicana was low even at comparatively low H2S concentrations. Furthermore, we show that food limitation affects the survival of P. mexicana pointing to energetically costly physiological adaptations to detoxify H2S.

Natural and sexual selection against immigrants maintains differentiation among micro-allopatric populations

Local adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and hence lead to speciation. But what mechanisms contribute to reproductive isolation among diverging populations? We tested for natural and sexual selection against immigrants in a fish species inhabiting (and adapting to) nonsulphidic surface habitats, sulphidic surface habitats and a sulphidic cave. Gene flow is strong among sample sites situated within the same habitat type, but low among divergent habitat types. Our results indicate that females of both sulphidic populations discriminate against immigrant males during mate choice. Furthermore, using reciprocal translocation experiments, we document natural selection against migrants between nonsulphidic and sulphidic habitats, whereas migrants between sulphidic cave and surface habitats did not exhibit increased mortality within the same time period. Consequently, both natural and sexual selection may contribute to isolation among parapatric populations, and selection against immigrants may be a powerful mechanism facilitating speciation among locally adapted populations even over very small spatial distances.

Genetic differentiation and selection against migrants in evolutionarily replicated extreme environments.

We investigated mechanisms of reproductive isolation in livebearing fishes (genus Poecilia) inhabiting sulfidic and nonsulfidic habitats in three replicate river drainages. Although sulfide spring fish convergently evolved divergent phenotypes, it was unclear if mechanisms of reproductive isolation also evolved convergently. Using microsatellites, we found strongly reduced gene flow between adjacent populations from different habitat types, suggesting that local adaptation to sulfidic habitats repeatedly caused the emergence of reproductive isolation. Reciprocal translocation experiments indicate strong selection against immigrants into sulfidic waters, but also variation among drainages in the strength of selection against immigrants into nonsulfidic waters. Mate choice experiments revealed the evolution of assortative mating preferences in females from nonsulfidic but not from sulfidic habitats. The inferred strength of sexual selection against immigrants (RIs) was negatively correlated with the strength of natural selection (RIm), a pattern that could be attributed to reinforcement, whereby natural selection strengthens behavioral isolation due to reduced hybrid fitness. Overall, reproductive isolation and genetic differentiation appear to be replicated and direct consequences of local adaptation to sulfide spring environments, but the relative contributions of different mechanisms of reproductive isolation vary across these evolutionarily independent replicates, highlighting both convergent and nonconvergent evolutionary trajectories of populations in each drainage.

Convergent life-history shifts: toxic environments result in big babies in two clades of poeciliids

The majority of studies on ecological speciation in animals have investigated the divergence caused by biotic factors like divergent food sources or predatory regimes. Here, we examined a system where ecological speciation can clearly be ascribed to abiotic environmental gradients of naturally occurring toxic hydrogen sulfide (H2S). In southern Mexico, two genera of livebearing fishes (Poeciliidae: Poecilia and Gambusia) thrive in various watercourses with different concentrations of H2S. Previous studies have revealed pronounced genetic differentiation between different locally adapted populations in one species (Poecilia mexicana), pointing towards incipient speciation. In the present study, we examined female reproductive life-history traits in two species pairs: Gambusia sexradiata (from a nonsulfidic and a sulfidic habitat) and Gambusia eurystoma (sulfide-endemic), as well as P. mexicana (nonsulfidic and sulfidic) and Poecilia sulphuraria (sulfide endemic). We found convergent divergence of life-history traits in response to sulfide; most prominently, extremophile poeciliids exhibit drastically increased offspring size coupled with reduced fecundity. Furthermore, within each genus, this trend increased with increasing sulfide concentrations and was most pronounced in the two endemic sulfur-adapted species. We discuss the adaptive significance of large offspring size in toxic environments and propose that divergent life-history evolution may promote further ecological divergence through isolation by adaptation.

Locally adapted fish populations maintain small-scale genetic differentiation despite perturbation by a catastrophic flood event

BackgroundLocal adaptation to divergent environmental conditions can promote population genetic differentiation even in the absence of geographic barriers and hence, lead to speciation. Perturbations by catastrophic events, however, can distort such parapatric ecological speciation processes. Here, we asked whether an exceptionally strong flood led to homogenization of gene pools among locally adapted populations of the Atlantic molly (Poecilia mexicana, Poeciliidae) in the Cueva del Azufre system in southern Mexico, where two strong environmental selection factors (darkness within caves and/or presence of toxic H2S in sulfidic springs) drive the diversification of P. mexicana. Nine nuclear microsatellites as well as heritable female life history traits (both as a proxy for quantitative genetics and for trait divergence) were used as markers to compare genetic differentiation, genetic diversity, and especially population mixing (immigration and emigration) before and after the flood.ResultsHabitat type (i.e., non-sulfidic surface, sulfidic surface, or sulfidic cave), but not geographic distance was the major predictor of genetic differentiation. Before and after the flood, each habitat type harbored a genetically distinct population. Only a weak signal of individual dislocation among ecologically divergent habitat types was uncovered (with the exception of slightly increased dislocation from the Cueva del Azufre into the sulfidic creek, El Azufre). By contrast, several lines of evidence are indicative of increased flood-induced dislocation within the same habitat type, e.g., between different cave chambers of the Cueva del Azufre.ConclusionsThe virtual absence of individual dislocation among ecologically different habitat types indicates strong natural selection against migrants. Thus, our current study exemplifies that ecological speciation in this and other systems, in which extreme environmental factors drive speciation, may be little affected by temporary perturbations, as adaptations to physico-chemical stressors may directly affect the survival probability in divergent habitat types.

Predation’s Role in Life-History Evolution of a Livebearing Fish and a Test of the Trexler-DeAngelis Model of Maternal Provisioning

Populations experiencing consistent differences in predation risk and resource availability are expected to follow divergent evolutionary trajectories. For example, live-history theory makes specific predictions for how predation should drive life-history evolution, and according to the Trexler-DeAngelis model for the evolution of matrotrophy, postfertilization maternal provisioning is most likely to evolve in environments with consistent, high levels of resource availability. Using the model system of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes with and without the piscivorous bigmouth sleeper (Gobiomorus dormitor), we provide some of the strongest tests of these predictions to date, as resource availability does not covary with predation regime in this system, and we examine numerous (14) isolated natural populations. We found clear evidence for the expected life-history divergence between predation regimes and empirical support of the Trexler-DeAngelis model. Moreover, based on molecular and lab-rearing data, our study offers strong evidence for convergent evolution of similar life histories in similar predation regimes, largely matching previous phenotypic patterns observed in other poeciliid lineages (Brachyrhaphis spp., Poecilia reticulata), and further supports the notion that matrotrophy is most likely to evolve in stable high-resource environments.

Female sperm limitation in natural populations of a sexual/asexual mating complex (Poecilia latipinna, Poecilia formosa)

In sperm-dependent sexual/asexual mating systems, male mate choice is critical for understanding the mechanisms behind apparent stability observed in natural populations. The gynogenetic Amazon molly (Poecilia formosa) requires sperm from sexual males (e.g. Poecilia latipinna) to trigger embryogenesis, but inheritance is strictly maternal. Consequently, males should try to avoid or reduce the cost of mating with asexuals. We investigated male mate choice by documenting the presence of sperm in natural populations and found that a higher proportion of sexual females had sperm than asexuals. In addition, among those females that had sperm, sexuals had more sperm than asexuals. Our results hint at a role for male mate choice as a stabilizing factor in such systems.

Colonisation of toxic environments drives predictable life-history evolution in livebearing fishes (Poeciliidae)

New World livebearing fishes (family Poeciliidae) have repeatedly colonised toxic, hydrogen sulphide-rich waters across their natural distribution. Physiological considerations and life-history theory predict that these adverse conditions should favour the evolution of larger offspring. Here, we examined nine poeciliid species that independently colonised toxic environments, and show that these fishes have indeed repeatedly evolved much larger offspring size at birth in sulphidic waters, thus uncovering a widespread pattern of predictable evolution. However, a second pattern, only indirectly predicted by theory, proved additionally common: a reduction in the number of offspring carried per clutch (i.e. lower fecundity). Our analyses reveal that this secondary pattern represents a mere consequence of a classic life-history trade-off combined with strong selection on offspring size alone. With such strong natural selection in extreme environments, extremophile organisms may commonly exhibit multivariate phenotypic shifts even though not all diverging traits necessarily represent adaptations to the extreme conditions.