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Scholarly Works (12 results)

  • Thesis
  • Peer Reviewed
UC Berkeley Electronic Theses and Dissertations (2022)

Evolutionary novelty may be an important driver of diversification, yet theory does not agree on the circumstances or processes that may lead to novelty in the first place. Current theory may be insufficient for explaining observed natural patterns because it does not consider the multivariate nature of novelty and instead makes predictions assuming that evolution occurs along a single axis. Furthermore, it is challenging to measure variation across many biological levels in a single focal organism, and there is consequently a lack of empirical data to inform new hypotheses. Here, I investigate evolutionary novelty within an adaptive radiation of Cyprinodon pupfish endemic to San Salvador Island, Bahamas. This radiation contains two fantastic examples of novelty in the snail-eating (C. brontotheroides) and scale-eating pupfish (C. desquamator), and contains a third generalist pupfish (C. variegatus) similar to outgroup populations.

In chapter one I investigate if shifts in behavior are associated with novelty in pupfish. I specifically test the aggression hypothesis, which suggests that scale-eating arose due to the incidental ingestion of scales during aggressive interactions and predicts that scale-eating pupfish should have the highest levels of aggression compared to all other species. I empirically tested this prediction and found that both scale- and snail-eating pupfish are more behaviorally aggressive than algae-eating or outgroup species and show differential expression in the same aggression related pathways compared to the generalist pupfish species. These results suggest that behavioral shifts are indeed associated with the evolution of novelty and may be adaptive for dietary specialization.

In chapters two and three I investigate the contributions of morphological and behavioral adaptations to scale- and snail-feeding performance. I developed a new method for measuring bite size (a proxy for scale-feeding performance) across pupfish species and found that scale-eating pupfish have a unique, behaviorally mediated, kinematic profile adaptive for taking large bites. The kinematic profiles of F1 scale-eating hybrids from this study were dissimilar to those of purebred scale-eaters—even for traits that are behaviorally mediated—suggesting that shifts in morphology and behavior are likely necessary for high performance in this niche. I also measured snail-eating performance between pupfish species, to determine if the novel nasal protrusion (morphology) of the snail-eating pupfish is adaptive for snail consumption. I found that snail-eaters, snail-eating hybrids, and generalist pupfish all exhibit similar levels of performance and observed no relationship between nasal protrusion size and performance. These chapters suggest that shifts along a single axis (e.g., behavior) may be sufficient to produce some instances of novelty, but that others may require shifts along several axes in order to be successful.

In chapter four I investigated the genetic underpinnings of adaptive behavioral and morphological traits for both snail- and scale-feeding, with the goal of identifying if unique genomic regions, alleles, or SNPs were associated with each instance of novelty. I investigated the genetic basis of 31 adaptive traits for scale- and snail-feeding using a QTL mapping approach in two pupfish populations. I found that similar genomic regions were associated with craniofacial traits, but that many of these shared regions affected different, but highly correlated traits. I also found evidence of increased levels of adaptive introgression within shared QTL regions, suggesting that: 1) there is a surprising amount of genetic flexibility when adapting to a novel niche, and 2) introgression may be important for this transition.

Ultimately, this dissertation research provides a new framework for studying the multivariate nature of novelty. By quantifying variation across behavioral, morphological, and genomic axes I documented that scale-feeding may require shifts along multiple axes while snail-feeding may only require behavioral shifts. This is one of the first studies to empirically document variation across multiple biological levels in the context of novelty and the patterns described above further emphasizes that hypotheses considering shifts along only a single axis are not sufficient for fully understanding evolutionary novelty.

    Cover page: The Cascading Effects of Novelty: How adaptation to a novel niche affects behavior, morphology, and genomics
    • Article
    • Peer Reviewed
    UC Berkeley Previously Published Works (2020)
    Dietary specialization on hard prey items, such as mollusks and crustaceans, is commonly observed in a diverse array of fish species. Many fish consume these types of prey by crushing the shell to consume the soft tissue within, but a few fishes extricate the soft tissue without breaking the shell using a method known as oral shelling. Oral shelling involves pulling a mollusc from its shell and it may be a way to subvert an otherwise insurmountable shell defence. However, the biomechanical requirements and potential adaptations for oral shelling are unknown. Here, we test the hypothesis that a novel nasal protrusion is an adaptation for oral shelling in the durophagous pupfish (Cyprinodon brontotheroides). We first demonstrate oral shelling in this species and then predict that a larger nasal protrusion would allow pupfish to consume larger snails. Durophagous pupfish are found within an endemic radiation of pupfish on San Salvador Island, Bahamas. We took advantage of closely related sympatric species and outgroups to test: (a) whether durophagous pupfish shell and consume more snails than other species, (b) if F1 and F2 durophagous hybrids consume similar amounts of snails as purebred durophagous pupfish, and (c) if nasal protrusion size in parental and hybrid populations increases the maximum size of consumed snails. We found that durophagous pupfish and their hybrids consumed the most snails, but did not find a strong association between nasal protrusion size and maximum snail size consumed within the parental or F2 hybrid population, suggesting that the size of their novel nasal protrusion does not provide a major benefit in oral shelling. Instead, we suggest that the nasal protrusion may increase feeding efficiency, act as a sensory organ, or is a sexually selected trait, and that a strong feeding preference may be most important for oral shelling.
      Cover page: Oral shelling within an adaptive radiation of pupfishes: Testing the adaptive function of a novel nasal protrusion and behavioural preference.
      • Article
      • Peer Reviewed
      UC Berkeley Previously Published Works (2024)
      Phenotypic covariation among suites of traits may constrain or promote diversification both within and between species, yet few studies have empirically tested this relationship. In this study, we investigate whether phenotypic covariation of craniofacial traits is associated with diversification in an adaptive radiation of pupfishes found only on San Salvador Island, Bahamas (SSI). The radiation includes generalist, durophagous, and lepidophagous species. We compared phenotypic variation and covariation (i.e., the P matrix) between (1) allopatric populations of generalist pupfish from neighboring islands and estuaries in the Caribbean, (2) SSI pupfish allopatric lake populations with only generalist pupfish, and (3) SSI lake populations containing the full radiation in sympatry. Additionally, we examine patterns observed in the P matrices of two independent lab-reared F2 hybrid crosses of the two most morphologically distinct members of the radiation to make inferences about the underlying mechanisms contributing to the variation in craniofacial traits in SSI pupfishes. We found that the P matrix of SSI allopatric generalist populations exhibited higher levels of mean trait correlation, constraints, and integration with simultaneously lower levels of flexibility compared to allopatric generalist populations on other Caribbean islands and sympatric populations of all three species on SSI. We also document that while many craniofacial traits appear to result from additive genetic effects, variation in key traits such as head depth, maxilla length, and lower jaw length may be produced via non-additive genetic mechanisms. Ultimately, this study suggests that differences in phenotypic covariation significantly contribute to producing and maintaining organismal diversity.
        Cover page: Phenotypic covariation predicts diversification in an adaptive radiation of pupfishes.
        • Article
        • Peer Reviewed
        UC Berkeley Previously Published Works (2020)
        The origins of novel trophic specialization, in which organisms begin to exploit resources for the first time, may be explained by shifts in behavior such as foraging preferences or feeding kinematics. One way to investigate behavioral mechanisms underlying ecological novelty is by comparing prey capture kinematics among species. We investigated the contribution of kinematics to the origins of a novel ecological niche for scale-eating within a microendemic adaptive radiation of pupfishes on San Salvador Island, Bahamas. We compared prey capture kinematics across three species of pupfish while they consumed shrimp and scales in the lab, and found that scale-eating pupfish exhibited peak gape sizes twice as large as in other species, but also attacked prey with a more obtuse angle between their lower jaw and suspensorium. We then investigated how this variation in feeding kinematics could explain scale-biting performance by measuring bite size (surface area removed) from standardized gelatin cubes. We found that a combination of larger peak gape and more obtuse lower jaw and suspensorium angles resulted in approximately 40% more surface area removed per strike, indicating that scale-eaters may reside on a performance optimum for scale biting. To test whether feeding performance could contribute to reproductive isolation between species, we also measured F1 hybrids and found that their kinematics and performance more closely resembled generalists, suggesting that F1 hybrids may have low fitness in the scale-eating niche. Ultimately, our results suggest that the evolution of strike kinematics in this radiation is an adaptation to the novel niche of scale eating.
          Cover page: Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche
          • Article
          • Peer Reviewed
          UC Berkeley Previously Published Works (2019)
          Behavioral changes in a new environment are often assumed to precede the origins of evolutionary novelties. Here, we examined whether an increase in aggression is associated with a novel scale-eating trophic niche within a recent radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. We measured aggression using multiple behavioral assays and used transcriptomic analyses to identify differentially expressed genes in aggression and other behavioral pathways across 3 sympatric species in the San Salvador radiation (generalist, snail-eating specialist, and scale-eating specialist) and 2 generalist outgroups. Surprisingly, we found increased behavioral aggression and differential expression of aggression-related pathways in both the scale-eating and snail-eating specialists, despite their independent evolutionary origins. Increased behavioral aggression varied across both sex and stimulus context in both species. Our results indicate that aggression is not unique to scale-eating specialists. Instead, selection may increase aggression in other contexts such as niche specialization in general or mate competition. Alternatively, increased aggression may result from indirect selection on craniofacial traits, pigmentation, or metabolism-all traits which are highly divergent, exhibit signs of selective sweeps, and are affected by aggression-related genetic pathways which are differentially expressed in this system. In conclusion, the evolution of a novel predatory trophic niche within a recent adaptive radiation does not have clear-cut behavioral origins as previously assumed, highlighting the multivariate nature of adaptation and the complex integration of behavior with other phenotypic traits.
            Cover page: The behavioral origins of novelty: did increased aggression lead to scale-eating in pupfishes?
            • Article
            • Peer Reviewed
            UC Berkeley Previously Published Works (2020)
            Dietary specialization on hard prey items, such as mollusks and crustaceans, is commonly observed in a diverse array of fish species. Many fish consume these types of prey by crushing the shell to consume the soft tissue within, but a few fishes extricate the soft tissue without breaking the shell using a method known as oral shelling. Oral shelling involves pulling a mollusc from its shell and it may be a way to subvert an otherwise insurmountable shell defence. However, the biomechanical requirements and potential adaptations for oral shelling are unknown. Here, we test the hypothesis that a novel nasal protrusion is an adaptation for oral shelling in the durophagous pupfish (Cyprinodon brontotheroides). We first demonstrate oral shelling in this species and then predict that a larger nasal protrusion would allow pupfish to consume larger snails. Durophagous pupfish are found within an endemic radiation of pupfish on San Salvador Island, Bahamas. We took advantage of closely related sympatric species and outgroups to test: (a) whether durophagous pupfish shell and consume more snails than other species, (b) if F1 and F2 durophagous hybrids consume similar amounts of snails as purebred durophagous pupfish, and (c) if nasal protrusion size in parental and hybrid populations increases the maximum size of consumed snails. We found that durophagous pupfish and their hybrids consumed the most snails, but did not find a strong association between nasal protrusion size and maximum snail size consumed within the parental or F2 hybrid population, suggesting that the size of their novel nasal protrusion does not provide a major benefit in oral shelling. Instead, we suggest that the nasal protrusion may increase feeding efficiency, act as a sensory organ, or is a sexually selected trait, and that a strong feeding preference may be most important for oral shelling.
              Cover page: Oral shelling within an adaptive radiation of pupfishes: Testing the adaptive function of a novel nasal protrusion and behavioural preference
              • Article
              • Peer Reviewed
              UC Berkeley Previously Published Works (2019)
              Behavioral changes in a new environment are often assumed to precede the origins of evolutionary novelties. Here, we examined whether an increase in aggression is associated with a novel scale-eating trophic niche within a recent radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. We measured aggression using multiple behavioral assays and used transcriptomic analyses to identify differentially expressed genes in aggression and other behavioral pathways across 3 sympatric species in the San Salvador radiation (generalist, snail-eating specialist, and scale-eating specialist) and 2 generalist outgroups. Surprisingly, we found increased behavioral aggression and differential expression of aggression-related pathways in both the scale-eating and snail-eating specialists, despite their independent evolutionary origins. Increased behavioral aggression varied across both sex and stimulus context in both species. Our results indicate that aggression is not unique to scale-eating specialists. Instead, selection may increase aggression in other contexts such as niche specialization in general or mate competition. Alternatively, increased aggression may result from indirect selection on craniofacial traits, pigmentation, or metabolism-all traits which are highly divergent, exhibit signs of selective sweeps, and are affected by aggression-related genetic pathways which are differentially expressed in this system. In conclusion, the evolution of a novel predatory trophic niche within a recent adaptive radiation does not have clear-cut behavioral origins as previously assumed, highlighting the multivariate nature of adaptation and the complex integration of behavior with other phenotypic traits.
                Cover page: The behavioral origins of novelty: did increased aggression lead to scale-eating in pupfishes?
                • Article
                • Peer Reviewed
                UC Berkeley Previously Published Works (2020)
                The origins of novel trophic specialization, in which organisms begin to exploit novel resources for the first time, may be explained by shifts in behavior such as foraging preferences or feeding kinematics. One way to investigate behavioral mechanisms underlying ecological novelty is by comparing prey capture kinematics among species. We investigated the contribution of kinematics to the origins of a novel ecological niche for scale-eating within a microendemic adaptive radiation of pupfishes on San Salvador Island, Bahamas. We compared prey capture kinematics across three species of pupfish while consuming shrimp and scales in the lab, and found that scale-eating pupfish exhibited peak gape sizes twice as large as other species, but also attacked prey with a more obtuse angle between their lower jaw and suspensorium. We then investigated how this variation in feeding kinematics could explain scale-biting performance by measuring bite size (surface area removed) from standardized gelatin cubes. We found that a combination of larger peak gape and more obtuse lower jaw and suspensorium angles resulted in approximately 40% more surface area removed per strike, indicating that scale-eaters may reside on a performance optimum for scale-biting. To test whether feeding performance could contribute to reproductive isolation between species, we also measured F1 hybrids and found that their kinematics and performance more closely resembled generalists, suggesting that F1 hybrids may have low fitness in the scale-eating niche. Ultimately, our results suggest that the evolution of strike kinematics in this radiation is an adaptation to the novel niche of scale-eating.
                  Cover page: Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche.
                  • Article
                  • Peer Reviewed
                  UC Berkeley Previously Published Works (2019)
                  Biologists are drawn to the most extraordinary adaptations in the natural world, often referred to as evolutionary novelties, yet rarely do we understand the microevolutionary context underlying the origins of novel traits, behaviors, or ecological niches. Here we discuss insights gained into the origins of novelty from a research program spanning biological levels of organization from genotype to fitness in Caribbean pupfishes. We focus on a case study of the origins of novel trophic specialists on San Salvador Island, Bahamas and place this radiation in the context of other rapid radiations. We highlight questions that can be addressed about the origins of novelty at different biological levels, such as measuring the isolation of novel phenotypes on the fitness landscape, locating the spatial and temporal origins of adaptive variation contributing to novelty, detecting dysfunctional gene regulation due to adaptive divergence, and connecting behaviors with novel traits. Evolutionary novelties are rare, almost by definition, and we conclude that integrative case studies can provide insights into this rarity relative to the dynamics of adaptation to more common ecological niches and repeated parallel speciation, such as the relative isolation of novel phenotypes on fitness landscapes and the transient availability of ecological, genetic, and behavioral opportunities.
                    Cover page: How to investigate the origins of novelty: insights gained from genetic, behavioral, and fitness perspectives
                    • Article
                    • Peer Reviewed
                    UC Berkeley Previously Published Works (2024)
                    Populations may adapt to similar environments via parallel or non-parallel genetic changes, but the frequency of these alternative mechanisms and underlying contributing factors are still poorly understood outside model systems. We used QTL mapping to investigate the genetic basis of highly divergent craniofacial traits between the scale-eater (Cyprinodon desquamator) and molluscivore (C. brontotheroides) pupfish adapting to two different hypersaline lake environments on San Salvador Island, Bahamas. We lab-reared F2 scale-eater x molluscivore intercrosses from two different lake populations, estimated linkage maps, scanned for significant QTL for 29 skeletal and craniofacial traits, female mate preference, and sex. We compared the location of QTL between lakes to quantify parallel and non-parallel genetic changes. We detected significant QTL for six craniofacial traits in at least one lake. However, nearly all shared QTL loci were associated with a different craniofacial trait within each lake. Therefore, our estimate of parallel evolution of craniofacial genetic architecture could range from one out of six identical trait QTL (low parallelism) to five out of six integrated trait QTL (high parallelism). We suggest that pleiotropy and trait integration can affect estimates of parallel evolution, particularly within rapid radiations. We also observed increased adaptive introgression in shared QTL regions, suggesting that gene flow contributed to parallel evolution. Overall, our results suggest that the same genomic regions may contribute to parallel adaptation across integrated suites of craniofacial traits, rather than specific traits, and highlight the need for a more expansive definition of parallel evolution.
                      Cover page: Parallel evolution of integrated craniofacial traits in trophic specialist pupfishes.
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