skip to main content


Title: Recent warming reduces the reproductive advantage of large size and contributes to evolutionary downsizing in nature
Body size is a key functional trait that is predicted to decline under warming. Warming is known to cause size declines via phenotypic plasticity, but evolutionary responses of body size to warming are poorly understood. To test for warming-induced evolutionary responses of body size and growth rates, we used populations of mosquitofish ( Gambusia affinis ) recently established (less than 100 years) from a common source across a strong thermal gradient (19–33°C) created by geothermal springs. Each spring is remarkably stable in temperature and is virtually closed to gene flow from other thermal environments. Field surveys show that with increasing site temperature, body size distributions become smaller and the reproductive advantage of larger body size decreases. After common rearing to reveal recently evolved trait differences, warmer-source populations expressed slowed juvenile growth rates and increased reproductive effort at small sizes. These results are consistent with an adaptive basis of the plastic temperature–size rule, and they suggest that temperature itself can drive the evolution of countergradient variation in growth rates. The rapid evolution of reduced juvenile growth rates and greater reproduction at a small size should contribute to substantial body downsizing in populations, with implications for population dynamics and for ecosystems in a warming world.  more » « less
Award ID(s):
1849227
NSF-PAR ID:
10219418
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Volume:
287
Issue:
1928
ISSN:
0962-8452
Page Range / eLocation ID:
20200608
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Body size influences an individual's physiology and the nature of its intra‐ and interspecific interactions. Changes in this key functional trait can therefore have important implications for populations as well. For example, among invertebrates, there is typically a positive correlation between female body size and reproductive output. Increasing body size can consequently trigger changes in population density, population structure (e.g. adult to juvenile ratio) and the strength of intraspecific competition.

    Body size changes have been documented in several species in the Arctic, a region that is warming rapidly. In particular, wolf spiders, one of the most abundant arctic invertebrate predators, are becoming larger and therefore more fecund. Whether these changes are affecting their populations and role within food webs is currently unclear.

    We investigated the population structure and feeding ecology of the dominant wolf spider speciesPardosa lapponicaat two tundra sites where adult spiders naturally differ in mean body size. Additionally, we performed a mesocosm experiment to investigate how variation in wolf spider density, which is likely to change as a function of body size, influences feeding ecology and its sensitivity to warming.

    We found that juvenile abundance is negatively associated with female size and that wolf spiders occupied higher trophic positions where adult females were larger. Because female body size is positively related to fecundity inP. lapponica, the unexpected finding of fewer juveniles with larger females suggests an increase in density‐dependent cannibalism as a result of increased intraspecific competition for resources. Higher rates of density‐dependent cannibalism are further supported by the results from our mesocosm experiment, in which individuals occupied higher trophic positions in plots with higher wolf spider densities. We observed no changes in wolf spider feeding ecology in association with short‐term experimental warming.

    Our results suggest that body size variation in wolf spiders is associated with variation in intraspecific competition, feeding ecology and population structure. Given the widespread distribution of wolf spiders in arctic ecosystems, body size shifts in these predators as a result of climate change could have implications for lower trophic levels and for ecosystem functioning.

     
    more » « less
  2. Abstract

    Predicted changes in global temperature are expected to increase extinction risk for ectotherms, primarily through increased metabolic rates. Higher metabolic rates generate increased maintenance energy costs which are a major component of energy budgets. Organisms often employ plastic or evolutionary (e.g., local adaptation) mechanisms to optimize metabolic rate with respect to their environment. We examined relationships between temperature and standard metabolic rate across four populations of a widespread amphibian species to determine if populations vary in metabolic response and if their metabolic rates are plastic to seasonal thermal cues. Populations from warmer climates lowered metabolic rates when acclimating to summer temperatures as compared to spring temperatures. This may act as an energy saving mechanism during the warmest time of the year. No such plasticity was evident in populations from cooler climates. Both juvenile and adult salamanders exhibited metabolic plasticity. Although some populations responded to historic climate thermal cues, no populations showed plastic metabolic rate responses to future climate temperatures, indicating there are constraints on plastic responses. We postulate that impacts of warming will likely impact the energy budgets of salamanders, potentially affecting key demographic rates, such as individual growth and investment in reproduction.

     
    more » « less
  3. Abstract

    Dispersal is a crucial component of species' responses to climate warming. Warming‐induced changes in species' distributions are the outcome of how temperature affects dispersal at the individual level. Yet, there is little or no theory that considers the temperature dependence of dispersal when investigating the impacts of warming on species' distributions.

    Here I take a first step towards filling this key gap in our knowledge. I focus on ectotherms, species whose body temperature depends on the environmental temperature, not least because they constitute the majority of biodiversity on the planet. I develop a mathematical model of spatial population dynamics that explicitly incorporates mechanistic descriptions of ectotherm life history trait responses to temperature. A novel feature of this framework is the explicit temperature dependence of all phases of dispersal: emigration, transfer and settlement.

    I report three key findings. First, dispersal, regardless of whether it is random or temperature‐dependent, allows both tropical and temperate ectotherms to track warming‐induced changes in their thermal environments and to expand their distributions beyond the lower and upper thermal limits of their respective climate envelopes. In the absence of dispersal mortality, warming does not alter these new distributional limits.

    Second, an analysis based solely on trait response data predicts that tropical ectotherms should be able to expand their distributions polewards to a greater degree than temperate ectotherms. Analysis of the dynamical model confirms this prediction. Tropical ectotherms have an advantage when moving to cooler climates because they experience lower within‐patch and dispersal mortality, and their higher thermal optima and maximal birth rates allow them to take advantage of the warmer parts of the year. Previous theory has shown that tropical ectotherms are more successful in invading and adapting the temperate climates than vice versa. This study provides the key missing piece, by showing how temperature‐dependent dispersal could facilitate both invasion and adaptation.

    Third, dispersal mortality does not affect the poleward expansion of ectotherm distributions. But, it prevents both tropical and temperate ectotherms from maintaining sink populations in localities that are too warm to be viable in the absence of dispersal. Dispersal mortality also affects species' abundance patterns, causing a larger decline in abundance throughout the range when species disperse randomly rather than in response to thermal habitat suitability. In this way, dispersal mortality can facilitate the evolution of dispersal modes that maximize fitness in warmer thermal environments.

     
    more » « less
  4. Cooke, Steve (Ed.)
    Abstract Models of species response to climate change often assume that physiological traits are invariant across populations. Neglecting potential intraspecific variation may overlook the possibility that some populations are more resilient or susceptible than others, creating inaccurate predictions of climate impacts. In addition, phenotypic plasticity can contribute to trait variation and may mediate sensitivity to climate. Quantifying such forms of intraspecific variation can improve our understanding of how climate can affect ecologically important species, such as invasive predators. Here, we quantified thermal performance (tolerance, acclimation capacity, developmental traits) across seven populations of the predatory marine snail (Urosalpinx cinerea) from native Atlantic and non-native Pacific coast populations in the USA. Using common garden experiments, we assessed the effects of source population and developmental acclimation on thermal tolerance and developmental traits of F1 snails. We then estimated climate sensitivity by calculating warming tolerance (thermal tolerance − habitat temperature), using field environmental data. We report that low-latitude populations had greater thermal tolerance than their high latitude counterparts. However, these same low-latitude populations exhibited decreased thermal tolerance when exposed to environmentally realistic higher acclimation temperatures. Low-latitude native populations had the greatest climate sensitivity (habitat temperatures near thermal limits). In contrast, invasive Pacific snails had the lowest climate sensitivity, suggesting that these populations are likely to persist and drive negative impacts on native biodiversity. Developmental rate significantly increased in embryos sourced from populations with greater habitat temperature but had variable effects on clutch size and hatching success. Thus, warming can produce widely divergent responses within the same species, resulting in enhanced impacts in the non-native range and extirpation in the native range. Broadly, our results highlight how intraspecific variation can alter management decisions, as this may clarify whether management efforts should be focused on many or only a few populations. 
    more » « less
  5. Abstract

    Species introductions provide opportunities to quantify rates and patterns of evolutionary change in response to novel environments. Alewives (Alosa pseudoharengus) are native to the East Coast of North America where they ascend coastal rivers to spawn in lakes and then return to the ocean. Some populations have become landlocked within the last 350 years and diverged phenotypically from their ancestral marine population. More recently, alewives were introduced to the Laurentian Great Lakes (~150 years ago), but these populations have not been compared to East Coast anadromous and landlocked populations. We quantified 95 years of evolution in foraging traits and overall body shape of Great Lakes alewives and compared patterns of phenotypic evolution of Great Lakes alewives to East Coast anadromous and landlocked populations. Our results suggest that gill raker spacing in Great Lakes alewives has evolved in a dynamic pattern that is consistent with responses to strong but intermittent eco‐evolutionary feedbacks with zooplankton size. Following their initial colonization of Lakes Ontario and Michigan, dense alewife populations likely depleted large‐bodied zooplankton, which drove a decrease in alewife gill raker spacing. However, the introduction of large, non‐native zooplankton to the Great Lakes in later decades resulted in an increase in gill raker spacing, and present‐day Great Lakes alewives have gill raker spacing patterns that are similar to the ancestral East Coast anadromous population. Conversely, contemporary Great Lakes alewife populations possess a gape width consistent with East Coast landlocked populations. Body shape showed remarkable parallel evolution with East Coast landlocked populations, likely due to a shared response to the loss of long‐distance movement or migrations. Our results suggest the colonization of a new environment and cessation of migration can result in rapid parallel evolution in some traits, but contingency also plays a role, and a dynamic ecosystem can also yield novel trait combinations.

     
    more » « less