Stage-Specific Demographic Effects of Hydrologic Variation in a Stream Salamander.

AbstractWe lack a strong understanding of how organisms with complex life histories respond to climate variation. Many stream-associated species have multistage life histories that are likely to influence the demographic consequences of floods and droughts. However, tracking stage-specific demographic responses requires high-resolution, long-term data that are rare. We used 8 years of capture-recapture data for the headwater stream salamander Gyrinophilus porphyriticus to quantify the effects of flooding and drying magnitude on stage-specific vital rates and population growth. Drying reduced larval recruitment but increased the probability of metamorphosis (i.e., adult recruitment). Flooding reduced adult recruitment but had no effect on larval recruitment. Larval and adult survival declined with flooding but were unaffected by drying. Annual population growth rates (λ) declined with flooding and drying. Lambda also declined over the study period (2012-2021), although mean λ was 1.0 over this period. Our results indicate that G. porphyriticus populations are resilient to hydrologic variation because of compensatory effects on recruitment of larvae versus adults (i.e., reproduction vs. metamorphosis). Complex life cycles may enable this resilience to climate variation by creating opportunities for compensatory demographic responses across stages. However, more frequent and intense hydrologic variation in the latter half of this study contributed to a decline in λ over time, suggesting that increasing environmental variability poses a threat even when demographic compensation occurs.

Outbreeding reduces survival during metamorphosis in a headwater stream salamander.

Assessing direct fitness effects of individual genetic diversity is challenging due to the intensive and long-term data needed to quantify survival and reproduction in the wild. But resolving these effects is necessary to determine how inbreeding and outbreeding influence eco-evolutionary processes. We used 8 years of capture-recapture data and single nucleotide polymorphism genotypes for 1906 individuals to test for effects of individual heterozygosity on stage-specific survival probabilities in the salamander Gyrinophilus porphyriticus. The life cycle of G. porphyriticus includes an aquatic larval stage followed by metamorphosis into a semi-aquatic adult stage. In our study populations, the larval stage lasts 6-10 years, metamorphosis takes several months, and lifespan can reach 20 years. Previous studies showed that metamorphosis is a sensitive life stage, leading us to predict that fitness effects of individual heterozygosity would occur during metamorphosis. Consistent with this prediction, monthly probability of survival during metamorphosis declined with multi-locus heterozygosity (MLH), from 0.38 at the lowest MLH (0.10) to 0.06 at the highest MLH (0.38), a reduction of 84%. Body condition of larvae also declined significantly with increasing MLH. These relationships were consistent in the three study streams. With evidence of localised inbreeding within streams, these results suggest that outbreeding disrupts adaptations in pre-metamorphic and metamorphic individuals to environmental gradients along streams, adding to evidence that headwater streams are hotspots of microgeographic adaptation. Our results also underscore the importance of incorporating life history in analyses of the fitness effects of individual genetic diversity and suggest that metamorphosis and similar discrete life stage transitions may be critical periods of viability selection.

Environmentally Associated Variation in Dispersal Distance Affects Inbreeding Risk in a Stream Salamander.

AbstractAvoiding inbreeding is considered a key driver of dispersal evolution, and dispersal distances should be especially important in mediating inbreeding risk because the likelihood of mating with relatives decreases with dispersal distance. However, a lack of direct data on dispersal distances has limited empirical tests of this prediction, particularly in the context of the multiple selective forces that can influence dispersal. Using the headwater stream salamander Gyrinophilus porphyriticus, we tested whether spatial variation in environmental conditions leads to differences in dispersal distances, resulting in spatial variation in the effect of dispersal on inbreeding risk. Using capture-recapture and population genomic data from five streams, we found that dispersal distances were greater in downstream reaches than upstream reaches. Inbreeding risk trended lower for dispersers than nondispersers in downstream reaches but not in upstream reaches. Furthermore, stream reaches did not differ in spatial patterns of individual relatedness, indicating that variation in inbreeding risk was in fact due to differences in dispersal distances. These results demonstrate that environmentally associated variation in dispersal distances can cause the inbreeding consequences of dispersal to vary at fine spatial scales. They also show that selective pressures other than inbreeding avoidance maintain phenotypic variation in dispersal, underscoring the importance of addressing alternative hypotheses in dispersal research.

Hydrologic variability contributes to reduced survival through metamorphosis in a stream salamander.

Changes in the amount, intensity, and timing of precipitation are increasing hydrologic variability in many regions, but we have little understanding of how these changes are affecting freshwater species. Stream-breeding amphibians-a diverse group in North America-may be particularly sensitive to hydrologic variability during aquatic larval and metamorphic stages. Here, we tested the prediction that hydrologic variability in streams decreases survival through metamorphosis in the salamander Gyrinophilus porphyriticus, reducing recruitment to the adult stage. Using a 20-y dataset from Merrill Brook, a stream in northern New Hampshire, we show that abundance of G. porphyriticus adults has declined by ∼50% since 1999, but there has been no trend in larval abundance. We then tested whether hydrologic variability during summers influences survival through metamorphosis, using capture-mark-recapture data from Merrill Brook (1999 to 2004) and from 4 streams in the Hubbard Brook Experimental Forest (2012 to 2014), also in New Hampshire. At both sites, survival through metamorphosis declined with increasing variability of stream discharge. These results suggest that hydrologic variability reduces the demographic resilience and adaptive capacity of G. porphyriticus populations by decreasing recruitment of breeding adults. They also provide insight on how increasing hydrologic variability is affecting freshwater species, and on the broader effects of environmental variability on species with vulnerable metamorphic stages.

Spatial capture-recapture reveals age- and sex-specific survival and movement in stream amphibians.

Life-history information sets the foundation for our understanding of ecology and conservation requirements. For many species, this information is lacking even for basic demographic rates such as survival and movement. When survival and movement estimates are available, they are often derived from mixed demographic groups and do not consider differences among life stages or sexes, which is critical, because life stages and sexes often contribute differentially to population dynamics. We used hierarchical models informed with spatial capture-mark-recapture data of Ascaphus montanus (Rocky Mountain tailed frog) in five streams and A. truei (coastal tailed frog) in one stream to estimate variation in survival and movement by sex and age, represented by size. By incorporating survival and movement into a single model, we were able to estimate both parameters with limited bias. Annual survival was similar between sexes of A. montanus [females = 0.885 (95% CI 0.614-1), males = 0.901 (0.657-1)], but was slightly higher for female A. truei [0.836 (0.560-0.993)] than for males [0.664 (0.354-0.962)]. Survival of A. montanus peaked at mid-age, suggesting that lower survival of young and actuarial senescence may influence population demographics. Our models suggest that younger A. montanus moved farther than older individuals, and that females moved farther than males in both species. Our results provide uncommon insight into age- and sex-specific rates of survival and movement that are crucial elements of life-history strategies and are important for modeling population growth and prescribing conservation actions.

Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout.

Hybridization between invasive and native species, a significant threat to worldwide biodiversity, is predicted to increase due to climate-induced expansions of invasive species. Long-term research and monitoring are crucial for understanding the ecological and evolutionary processes that modulate the effects of invasive species. Using a large, multidecade genetics dataset (N = 582 sites, 12,878 individuals) with high-resolution climate predictions and extensive stocking records, we evaluate the spatiotemporal dynamics of hybridization between native cutthroat trout and invasive rainbow trout, the world's most widely introduced invasive fish, across the Northern Rocky Mountains of the United States. Historical effects of stocking and contemporary patterns of climatic variation were strongly related to the spread of hybridization across space and time. The probability of occurrence, extent of, and temporal changes in hybridization increased at sites in close proximity to historical stocking locations with greater rainbow trout propagule pressure, warmer water temperatures, and lower spring precipitation. Although locations with warmer water temperatures were more prone to hybridization, cold sites were not protected from invasion; 58% of hybridized sites had cold mean summer water temperatures (<11°C). Despite cessation of stocking over 40 years ago, hybridization increased over time at half (50%) of the locations with long-term data, the vast majority of which (74%) were initially nonhybridized, emphasizing the chronic, negative impacts of human-mediated hybridization. These results show that effects of climate change on biodiversity must be analyzed in the context of historical human impacts that set ecological and evolutionary trajectories.

Network analysis reveals multiscale controls on streamwater chemistry.

By coupling synoptic data from a basin-wide assessment of streamwater chemistry with network-based geostatistical analysis, we show that spatial processes differentially affect biogeochemical condition and pattern across a headwater stream network. We analyzed a high-resolution dataset consisting of 664 water samples collected every 100 m throughout 32 tributaries in an entire fifth-order stream network. These samples were analyzed for an exhaustive suite of chemical constituents. The fine grain and broad extent of this study design allowed us to quantify spatial patterns over a range of scales by using empirical semivariograms that explicitly incorporated network topology. Here, we show that spatial structure, as determined by the characteristic shape of the semivariograms, differed both among chemical constituents and by spatial relationship (flow-connected, flow-unconnected, or Euclidean). Spatial structure was apparent at either a single scale or at multiple nested scales, suggesting separate processes operating simultaneously within the stream network and surrounding terrestrial landscape. Expected patterns of spatial dependence for flow-connected relationships (e.g., increasing homogeneity with downstream distance) occurred for some chemical constituents (e.g., dissolved organic carbon, sulfate, and aluminum) but not for others (e.g., nitrate, sodium). By comparing semivariograms for the different chemical constituents and spatial relationships, we were able to separate effects on streamwater chemistry of (i) fine-scale versus broad-scale processes and (ii) in-stream processes versus landscape controls. These findings provide insight on the hierarchical scaling of local, longitudinal, and landscape processes that drive biogeochemical patterns in stream networks.

Vive la résistance: genome-wide selection against introduced alleles in invasive hybrid zones.

Evolutionary and ecological consequences of hybridization between native and invasive species are notoriously complicated because patterns of selection acting on non-native alleles can vary throughout the genome and across environments. Rapid advances in genomics now make it feasible to assess locus-specific and genome-wide patterns of natural selection acting on invasive introgression within and among natural populations occupying diverse environments. We quantified genome-wide patterns of admixture across multiple independent hybrid zones of native westslope cutthroat trout and invasive rainbow trout, the world's most widely introduced fish, by genotyping 339 individuals from 21 populations using 9380 species-diagnostic loci. A significantly greater proportion of the genome appeared to be under selection favouring native cutthroat trout (rather than rainbow trout), and this pattern was pervasive across the genome (detected on most chromosomes). Furthermore, selection against invasive alleles was consistent across populations and environments, even in those where rainbow trout were predicted to have a selective advantage (warm environments). These data corroborate field studies showing that hybrids between these species have lower fitness than the native taxa, and show that these fitness differences are due to selection favouring many native genes distributed widely throughout the genome.

Dispersal and selection mediate hybridization between a native and invasive species.

Hybridization between native and non-native species has serious biological consequences, but our understanding of how dispersal and selection interact to influence invasive hybridization is limited. Here, we document the spread of genetic introgression between a native (Oncorhynchus clarkii) and invasive (Oncorhynchus mykiss) trout, and identify the mechanisms influencing genetic admixture. In two populations inhabiting contrasting environments, non-native admixture increased rapidly from 1984 to 2007 and was driven by surprisingly consistent processes. Individual admixture was related to two phenotypic traits associated with fitness: size at spawning and age of juvenile emigration. Fish with higher non-native admixture were larger and tended to emigrate at a younger age--relationships that are expected to confer fitness advantages to hybrid individuals. However, strong selection against non-native admixture was evident across streams and cohorts (mean selection coefficient against genotypes with non-native alleles (s) = 0.60; s.e. = 0.10). Nevertheless, hybridization was promoted in both streams by the continuous immigration of individuals with high levels of non-native admixture from other hybrid source populations. Thus, antagonistic relationships between dispersal and selection are mediating invasive hybridization between these fish, emphasizing that data on dispersal and natural selection are needed to fully understand the dynamics of introgression between native and non-native species.

Partitioning the non-consumptive effects of predators on prey with complex life histories.

Non-consumptive effects (NCEs) of predators on prey can be as strong as consumptive effects (CEs) and may be driven by numerous mechanisms, including predator characteristics. Previous work has highlighted the importance of predator characteristics in predicting NCEs, but has not addressed how complex life histories of prey could mediate predator NCEs. We conducted a meta-analysis to compare the effects of predator gape limitation (gape limited or not) and hunting mode (active or sit-and-pursue) on the activity, larval period, and size at metamorphosis of larval aquatic amphibians and invertebrates. Larval prey tended to reduce their activity and require more time to reach metamorphosis in the presence of all predator functional groups, but the responses did not differ from zero. Prey metamorphosed at smaller size in response to non-gape-limited, active predators, but counter to expectations, prey metamorphosed larger when confronted by non-gape-limited, sit-and-pursue predators. These results indicate NCEs on larval prey life history can be strongly influenced by predator functional characteristics. More broadly, our results suggest that understanding predator NCEs would benefit from greater consideration of how prey life history attributes mediate population and community-level outcomes.

Individual growth rates and size at metamorphosis increase with watershed area in a stream salamander.

A fundamental goal of ecology is to understand how the physical environment influences intraspecific variability in life history and, consequently, fitness. In streams, discharge and associated habitat conditions change along a continuum from intermittency to permanence: Headwater streams typically have smaller watersheds and are thus more prone to drying than higher-order streams with larger watersheds and more consistent discharge. However, few empirical studies have assessed life history and associated population responses to this continuum in aquatic organisms. We tested the prediction that individual growth, rate of development, and population growth increase with watershed area in the long-lived stream salamander Gyrinophilus porphyriticus, where we use watershed area as a proxy for hydrologic intermittence. To address this hypothesis, we used 8 years of mark-recapture data from 53 reaches across 10 headwater streams in New Hampshire, USA. Individual growth rates and mean size at metamorphosis increased with watershed area for watersheds from 0.12 to 1.66 km2 . Population growth rates increased with watershed area; however, this result was not statistically significant at our sample size. Mean age of metamorphosis did not vary across watershed areas. Lower individual growth rates and smaller sizes at metamorphosis likely contributed to reduced lifetime fecundity and population growth in reaches with the smallest watershed areas and highest vulnerability to drought. These responses suggest that as droughts increase due to climate change, headwater specialists in hydrologically intermittent environments will experience a reduction in fitness due to smaller body sizes or other growth-related mechanisms.

Interactive effects of wildfire, forest management, and isolation on amphibian and parasite abundance.

Projected increases in wildfire and other climate-driven disturbances will affect populations and communities worldwide, including host-parasite relationships. Research in temperate forests has shown that wildfire can negatively affect amphibians, but this research has occurred primarily outside of managed landscapes where interactions with human disturbances could result in additive or synergistic effects. Furthermore, parasites represent a large component of biodiversity and can affect host fitness and population dynamics, yet they are rarely included in studies of how vertebrate hosts respond to disturbance. To determine how wildfire affects amphibians and their parasites, and whether effects differ between protected and managed landscapes, we compared abundance of two amphibians and two nematodes relative to wildfire extent and severity around wetlands in neighboring protected and managed forests (Montana, USA). Population sizes of adult, male long-toed salamanders (Ambystoma macrodactylum) decreased with increased burn severity, with stronger negative effects on isolated populations and in managed forests. In contrast, breeding population sizes of Columbia spotted frogs (Rana luteiventris) increased with burn extent in both protected and managed protected forests. Path analysis showed that the effects of wildfire on the two species of nematodes were consistent with differences in their life history and transmission strategies and the responses of their hosts. Burn severity indirectly reduced abundance of soil-transmitted Cosmocercoides variabilis through reductions in salamander abundance. Burn severity also directly reduced C. variabilis abundance, possibly though changes in soil conditions. For the aquatically transmitted nematode Gyrinicola batrachiensis, the positive effect of burn extent on density of Columbia spotted frog larvae indirectly increased parasite abundance. Our results show that effects of wildfire on amphibians depend upon burn extent and severity, isolation, and prior land use. Through subsequent effects on the parasites, our results also reveal how changes in disturbance regimes can affect communities across trophic levels.

Rapid increases and time-lagged declines in amphibian occupancy after wildfire.

Climate change is expected to increase the frequency and severity of drought and wildfire. Aquatic and moisture-sensitive species, such as amphibians, may be particularly vulnerable to these modified disturbance regimes because large wildfires often occur during extended droughts and thus may compound environmental threats. However, understanding of the effects of wildfires on amphibians in forests with long fire-return intervals is limited. Numerous stand-replacing wildfires have occurred since 1988 in Glacier National Park (Montana, U.S.A.), where we have conducted long-term monitoring of amphibians. We measured responses of 3 amphibian species to fires of different sizes, severity, and age in a small geographic area with uniform management. We used data from wetlands associated with 6 wildfires that burned between 1988 and 2003 to evaluate whether burn extent and severity and interactions between wildfire and wetland isolation affected the distribution of breeding populations. We measured responses with models that accounted for imperfect detection to estimate occupancy during prefire (0-4 years) and different postfire recovery periods. For the long-toed salamander (Ambystoma macrodactylum) and Columbia spotted frog (Rana luteiventris), occupancy was not affected for 6 years after wildfire. But 7-21 years after wildfire, occupancy for both species decreased ≥ 25% in areas where >50% of the forest within 500 m of wetlands burned. In contrast, occupancy of the boreal toad (Anaxyrus boreas) tripled in the 3 years after low-elevation forests burned. This increase in occupancy was followed by a gradual decline. Our results show that accounting for magnitude of change and time lags is critical to understanding population dynamics of amphibians after large disturbances. Our results also inform understanding of the potential threat of increases in wildfire frequency or severity to amphibians in the region.

Use of multiple dispersal pathways facilitates amphibian persistence in stream networks.

Although populations of amphibians are declining worldwide, there is no evidence that salamanders occupying small streams are experiencing enigmatic declines, and populations of these species seem stable. Theory predicts that dispersal through multiple pathways can stabilize populations, preventing extinction in habitat networks. However, empirical data to support this prediction are absent for most species, especially those at risk of decline. Our mark-recapture study of stream salamanders reveals both a strong upstream bias in dispersal and a surprisingly high rate of overland dispersal to adjacent headwater streams. This evidence of route-dependent variation in dispersal rates suggests a spatial mechanism for population stability in headwater-stream salamanders. Our results link the movement behavior of stream salamanders to network topology, and they underscore the importance of identifying and protecting critical dispersal pathways when addressing region-wide population declines.

Source-sink dynamics within a complex life history.

Source-sink patch dynamics occur when movement from sources stabilizes sinks by compensating for low local vital rates. The mechanisms underlying source-sink dynamics may be complicated in species that undergo transitions between discrete life stages, particularly when stages have overlapping habitat requirements and similar movement abilities. In these species, for example, the demographic effects of movement by one stage may augment or offset the effects of movement by another stage. We used a stream salamander system to investigate patch dynamics within this form of complex life history. Specifically, we tested the hypothesis that the salamander Gyrinophilus porphyriticus experiences source-sink dynamics in riffles and pools, the dominant geomorphic patch types in headwater streams. We estimated stage-specific survival probabilities in riffles and pools and stage-specific movement probabilities between the two patch types using 8 years of capture-recapture data on 4491 individuals, including premetamorphic larvae and postmetamorphic adults. We then incorporated survival and movement probabilities into a stage-structured, two-patch model to determine the demographic interactions between riffles and pools. Monthly survival probabilities of both stages were higher in pools than in riffles. Larvae were more likely to move from riffles to pools, but adults were more likely to move from pools to riffles, despite experiencing much lower survival in riffles. In simulations, eliminating interpatch movements by both stages indicated that riffles are sinks that rely on immigration from pools for stability. Allowing only larvae to move stabilized both patch types, but allowing only adults to move destabilized pools due to the demographic cost of adult emigration. These results indicated that larval movement not only stabilizes riffles, but also offsets the destabilizing effects of maladaptive adult movement. Similar patch dynamics may emerge in any structured population in which movement and local vital rates differ by age, size, or stage. Addressing these forms of internal demographic structure in patch dynamics analyses will help to refine and advance general understanding of spatial ecology.

Linking extinction-colonization dynamics to genetic structure in a salamander metapopulation.

Theory predicts that founder effects have a primary role in determining metapopulation genetic structure. However, ecological factors that affect extinction-colonization dynamics may also create spatial variation in the strength of genetic drift and migration. We tested the hypothesis that ecological factors underlying extinction-colonization dynamics influenced the genetic structure of a tiger salamander (Ambystoma tigrinum) metapopulation. We used empirical data on metapopulation dynamics to make a priori predictions about the effects of population age and ecological factors on genetic diversity and divergence among 41 populations. Metapopulation dynamics of A. tigrinum depended on wetland area, connectivity and presence of predatory fish. We found that newly colonized populations were more genetically differentiated than established populations, suggesting that founder effects influenced genetic structure. However, ecological drivers of metapopulation dynamics were more important than age in predicting genetic structure. Consistent with demographic predictions from metapopulation theory, genetic diversity and divergence depended on wetland area and connectivity. Divergence was greatest in small, isolated wetlands where genetic diversity was low. Our results show that ecological factors underlying metapopulation dynamics can be key determinants of spatial genetic structure, and that habitat area and isolation may mediate the contributions of drift and migration to divergence and evolution in local populations.

Decoupling of genetic and phenotypic divergence in a headwater landscape.

In stream organisms, the landscape affecting intraspecific genetic and phenotypic divergence is comprised of two fundamental components: the stream network and terrestrial matrix. These components are known to differentially influence genetic structure in stream species, but to our knowledge, no study has compared their effects on genetic and phenotypic divergence. We examined how the stream network and terrestrial matrix affect genetic and phenotypic divergence in two stream salamanders, Gyrinophilus porphyriticus and Eurycea bislineata, in the Hubbard Brook Watershed, New Hampshire, USA. On the basis of previous findings and differences in adult terrestriality, we predicted that genetic divergence and phenotypic divergence in body morphology would be correlated in both species, but structured primarily by distance along the stream network in G. porphyriticus, and by overland distance in E. bislineata. Surprisingly, spatial patterns of genetic and phenotypic divergence were not strongly correlated. Genetic divergence, based on amplified DNA fragment length polymorphisms, increased with absolute geographic distance between sites. Phenotypic divergence was unrelated to absolute geographic distance, but related to relative stream vs. overland distances. In G. porphyriticus, phenotypic divergence was low when sites were close by stream distance alone and high when sites were close by overland distance alone. The opposite was true for E. bislineata. These results show that small differences in life history can produce large differences in patterns of intraspecific divergence, and the limitations of landscape genetic data for inferring phenotypic divergence. Our results also underscore the importance of explicitly comparing how terrestrial and aquatic conditions affect spatial patterns of divergence in species with biphasic life cycles.

Differences in Corticosterone Release Rates of Larval Spring Salamanders (Gyrinophilus porphyriticus) in Response to Native Fish Presence.

Invasive fish predators are an important factor causing amphibian declines and may have direct and indirect effects on amphibian survival. For example, early non-lethal exposure to these stressors may reduce survival in later life stages, especially in biphasic species. In amphibians, the glucocorticoid hormone corticosterone is released by the hypothalamo-pituitary-interrenal axis (HPI), as an adaptive physiological response to environmental stressors. The corticosterone response (baseline and response to acute stressors) is highly flexible and context dependent, and this variation can allow individuals to alter their phenotype and behavior with environmental changes, ultimately increasing survival. We sampled larvae of the spring salamander (Gyrinophilus porphyriticus) from two streams that each contained predatory brook trout (Slavelinus fontinalis) in the lower reaches and no predatory brook trout in the upper reaches. We measured baseline and stress-induced corticosterone release rates of larvae from the lower and upper reaches using a non-invasive water-borne hormone assay. We hypothesized that corticosterone release rates would differ between larvae from fish-present reaches and larvae from fish-free reaches. We found that baseline and stressor-induced corticosterone release rates were downregulated in larvae from reaches with fish predators. These results indicate that individuals from reaches with predatory trout are responding to fish predators by downregulating corticosterone while maintaining an active HPI axis. This may allow larvae more time to grow before metamorphosing, while also allowing them to physiologically respond to novel stressors. However, prolonged downregulation of corticosterone release rates can impact growth in post-metamorphic individuals.

Sex-related differences in aging rate are associated with sex chromosome system in amphibians.

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture-recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the "unguarded X/Z effect") or repeat-rich Y/W chromosome (the "toxic Y/W effect") could accelerate aging in the heterogametic sex in some vertebrate clades.