The establishment of reproductive barriers between populations can fuel the evolution of new species. A genetic framework for this process posits that “incompatible” interactions between genes can evolve that result in reduced survival or reproduction in hybrids. However, progress has been slow in identifying individual genes that underlie hybrid incompatibilities. We used a combination of approaches to map the genes that drive the development of an incompatibility that causes melanoma in swordtail fish hybrids. One of the genes involved in this incompatibility also causes melanoma in hybrids between distantly related species. Moreover, this melanoma reduces survival in the wild, likely because of progressive degradation of the fin. This work identifies genes underlying a vertebrate hybrid incompatibility and provides a glimpse into the action of these genes in natural hybrid populations.

The establishment of reproductive barriers between populations is the key process that fuels the evolution of new species. A genetic framework for this process was proposed over 80 years ago, which posits “incompatible” interactions between genes that result in reduced survival or reproduction in hybrids. Despite this foundational work, progress has been slow in identifying individual genes that underlie hybrid incompatibilities, with only a handful known to date. Here, we use a combination of approaches to precisely map the genes that drive the development of a melanoma incompatibility in swordtail fish hybrids. We find that one of the genes involved in this incompatibility also causes melanoma in hybrids between distantly related species. Moreover, we show that this melanoma reduces survival in the wild, likely due to progressive degradation of the fin. Together, this work represents only the second case where the genes underlying a vertebrate hybrid incompatibility have been identified and provides the first glimpse into the action of these genes in natural hybrid populations.One sentence summaryUsing a combination of mapping approaches, we identify interacting genes that lead to melanoma in hybrids and characterize their effects in natural hybrid populations.

Evolution has shaped social dynamics across species to resolve aggressive interactions with as little physical fighting as possible, balancing the potential value of the resources gained against the cost of suffering injury or death (Holekamp & Strauss, 2016;Maynard Smith & Harper, 1988;van Staaden et al., 2011). Aggressive behavior, through either physical or non-physical acts, is used to resolve conflicts related to access to resources such as food, shelter, territory, and mates. Extraordinary diversity exists in how different species express aggression. For example, body size is a reliable predictor of contest intensity in fish relying on visual displays (Moretz, 2003;Reddon et al., 2011), whereas in frogs, in which displays are primarily auditory, body size is generally unrelated to the duration or escalation of aggressive interactions (Owen & Gordon, 2005; Reichert & Gerhardt, 2011). Even members of the same species alter

Natural selection shapes traits during evolution including animal coloration known to be important for concealment and communication and color has been particularly salient in the explosive radiation of cichlid fish species in the rift valley lakes of East Africa. Though selection can produce variation in color via genetic substrates during early development, plasticity in coloration can occur through endocrine, neural, and transcriptional cues in response to various environmental stimuli. It is well known that some animals often change color to match their visual ecology. Adult male cichlid fish (Astatotilapia burtoni, Lake Tanganyika) can switch between blue and yellow body colors. Different colors result from the expression of pigment-bearing cells, which differ in density and function between these two color morphs. We show that A. burtoni switches from yellow to blue depending on their visual environment by downregulating endothelin receptor B (EdnRB) mRNA via DNA hypermethylation at a single cytosine residue within its promoter. EdnRB functions in yellow chromatophores to signal the aggregation of yellow pigments, making yellow less visible. Taken together, the regulation of EdnRB through DNA methylation in yellow chromatophores, in part, contribute to pigmentation changes from blue to yellow, depending on the visual environment.

Social rank in a hierarchy determines which individuals have access to important resources such as food, shelter, and mates. In the African cichlid fish Astatotilapia burtoni, rank is under social control, such that larger males are more likely than smaller males to be dominant in rank. Although it is well known that the relative size of A. burtoni males is critical in controlling social rank, the specific behavioral strategies underlying responses to males of different sizes are not well understood. In this research, our goal was to characterize these responses by performing resident-intruder assays, in which aggressive behaviors were measured in territorial males in response to the introduction of unfamiliar males that differed in relative standard length (SL). We found that the relative SL of intruders played an important role in determining behavioral performance. Resident males exposed to larger (>5% larger in SL) or matched (between 0 and 5% larger or smaller in SL) intruder males performed more lateral displays, a type of non-physical aggression, compared to resident males exposed to smaller (>5% smaller in SL) intruder males. However, physical aggression, such as chases and bites, did not differ as a function of relative SL. Our results suggest that A. burtoni males amplify non-physical aggression to settle territorial disputes in response to differences in relative SL that were not previously considered to be behaviorally relevant.HighlightsRelative size determines social rank in the African cichlid Astatotilapia burtoniResident male A. burtoni respond differently to small size differences in intruder malesResidents perform more non-physical aggression against larger intrudersResidents do not alter physical aggression as a function of differently sized intrudersDistinct behavioral strategies are used against different intruders