skip to main content


Title: Biogeography of shell morphology in over‐exploited shellfish reveals adaptive trade‐offs on human‐inhabited islands and incipient selectively driven lineage bifurcation
Abstract Aim

Humans are unintentionally affecting the evolution of fishery species directly through exploitation and indirectly by altering climate. We aim to test for a relationship between biogeographic patterns in the shell phenotypes of an over‐exploited shellfish and the presence of humans to identify human‐mediated adaptive trade‐offs. The implications of these trade‐offs are discussed with respect to the sustainability of the fishery.

Taxon

The endemic Hawaiian intertidal limpet, ‘opihi makaiauli (Patellagastropoda, Nacellidae, Cellana exarata)

Methods

We surveyed phenotypic characters associated with temperature and predation avoidance across the entire species range and tested for differences in the relationship between these characters and latitude, on islands with and without humans.

Results

Among all limpets surveyed, there was a bimodal distribution in shell colour (light, dark) and a parapatric pattern of shell coloration across the archipelago with lighter shells being prevalent on the uninhabited islands and darker, more camouflaged shells being prevalent on the inhabited islands. On the cooler, uninhabited islands, all morphometric characters associated with thermal avoidance (surface area, height and doming) increased with decreasing latitude. On the hotter, inhabited islands, however, shells were flatter, less variable and less adapted for avoiding thermal stress than predation.

Main Conclusions

The biogeographic patterns in shell phenotype and previous genetic studies suggest that the population is beginning to bifurcate in response to disruptive and directional selection as well as geographic isolation between the islands with and without humans. Decreased phenotypic and genetic diversity on the inhabited islands despite much larger populations of ‘opihi suggests a prominent historical bottleneck. The prevalence of maladaptive dark, flat phenotypes for thermal avoidance on the inhabited islands suggests that predation is a stronger selective force, driving adaptive trade‐offs in shape and colour. We propose that this is likely a case of fisheries‐induced evolution and a millennium of harvesting is the most likely selective pressure driving the observed biogeographic patterns in shell morphology. The flatter, darker shells will allow body temperatures to rise higher in direct sunlight, therefore we hypothesize that the thermal niche of ‘opihi is narrower on inhabited islands and will continue to narrow as Earth warms.

 
more » « less
Award ID(s):
1743711
NSF-PAR ID:
10457645
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Biogeography
Volume:
47
Issue:
7
ISSN:
0305-0270
Page Range / eLocation ID:
p. 1494-1509
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Inducible prey defences occur when organisms undergo plastic changes in phenotype to reduce predation risk. When predation pressure varies persistently over space or time, such as when predator and prey co‐occur over only part of their biogeographic ranges, prey populations can become locally adapted in their inducible defences. In California estuaries, native Olympia oyster (Ostrea lurida) populations have evolved disparate phenotypic responses to an invasive predator, the Atlantic oyster drill (Urosalpinx cinerea). In this study, oysters from an estuary with drills, and oysters from an estuary without drills, were reared for two generations in a laboratory common garden, and subsequently exposed to cues from Atlantic drills. Comparative proteomics was then used to investigate molecular mechanisms underlying conserved and divergent aspects of their inducible defences. Both populations developed smaller, thicker, and harder shells after drill exposure, and these changes in shell phenotype were associated with upregulation of calcium transport proteins that could influence biomineralization. Inducible defences evolve in part because defended phenotypes incur fitness costs when predation risk is low. Immune proteins were downregulated by both oyster populations after exposure to drills, implying a trade‐off between biomineralization and immune function. Following drill exposure, oysters from the population that co‐occurs with drills grew smaller shells than oysters inhabiting the estuary not yet invaded by the predator. Variation in the response to drills between populations was associated with isoform‐specific protein expression. This trend suggests that a stronger inducible defence response evolved in oysters that co‐occur with drills through modification of an existing mechanism.

     
    more » « less
  2. Abstract

    Spatiotemporal variation in predation risk arises from interactions between landscape heterogeneity, predator densities and predator hunting mode, generating landscapes of fear for prey species that can have important effects on prey behaviour and ecosystem dynamics.

    As widespread apex predators, humans present a significant source of risk for hunted animal populations. Spatiotemporal patterns of risk from hunters can overlap or contrast with patterns of risk from other predators. Human infrastructure can also reshape spatial patterns of risk by facilitating or impeding hunter or predator movement, or deterring predators that are themselves wary of humans.

    We examined how anthropogenic and natural landscape features interact with hunting modes of rifle hunters and mountain lionsPuma concolorto generate spatiotemporal patterns of risk for their primary prey. We explored the implications of human‐modified landscapes of fear for Columbian black‐tailed deerOdocoileus hemionus columbianusin Mendocino County, California. We used historical harvest records, hunter GPS trackers and camera trap records of mountain lions to model patterns of risk for deer. We then used camera traps to examine deer spatial and temporal activity patterns in response to this variation in risk.

    Hunters and mountain lions exhibited distinct, contrasting patterns of spatiotemporal activity. Risk from rifle hunters, who rely on long lines of sight, was highest in open grasslands and near roads and was confined to the daytime. Risk from mountain lions, an ambush predator, was highest in dense shrubland habitat, farther from developed areas, and during the night and crepuscular periods. Areas of human settlement provided a refuge from both hunters and mountain lions. We found no evidence that deer avoided risk in space at the scale of our observations, but deer adjusted their temporal activity patterns to reduce the risk of encounters with humans and mountain lions in areas of higher risk.

    Our study demonstrates that interactions between human infrastructure, habitat cover and predator hunting mode can result in distinct spatial patterns of predation risk from hunters and other predators that may lead to trade‐offs for prey species. However, distinct diel activity patterns of predators may create vacant hunting domains that reduce costly trade‐offs for prey. Our study highlights the importance of temporal partitioning as a mechanism of predation risk avoidance.

     
    more » « less
  3. Abstract

    Fishing pressure on coral reef ecosystems has been frequently linked to reductions of large fishes and reef fish biomass. Associated impacts on overall community structure are, however, less clear. In size‐structured aquatic ecosystems, fishing impacts are commonly quantified using size spectra, which describe the distribution of individual body sizes within a community. We examined the size spectra and biomass of coral reef fish communities at 38US‐affiliated Pacific islands that ranged in human presence from near pristine to human population centers. Size spectra ‘steepened’ steadily with increasing human population and proximity to market due to a reduction in the relative biomass of large fishes and an increase in the dominance of small fishes. Reef fish biomass was substantially lower on inhabited islands than uninhabited ones, even at inhabited islands with the lowest levels of human presence. We found that on populated islands size spectra exponents decreased (analogous to size spectra steepening) linearly with declining biomass, whereas on uninhabited islands there was no relationship. Size spectra were steeper in regions of low sea surface temperature but were insensitive to variation in other environmental and geomorphic covariates. In contrast, reef fish biomass was highly sensitive to oceanographic conditions, being influenced by both oceanic productivity and sea surface temperature. Our results suggest that community size structure may be a more robust indicator than fish biomass to increasing human presence and that size spectra are reliable indicators of exploitation impacts across regions of different fish community compositions, environmental drivers, and fisheries types. Size‐based approaches that link directly to functional properties of fish communities, and are relatively insensitive to abiotic variation across biogeographic regions, offer great potential for developing our understanding of fishing impacts in coral reef ecosystems.

     
    more » « less
  4. Abstract Aim

    Are different fruit colours related to large‐scale patterns of dispersal, distribution and diversification? Here, we investigate this question for the first time, using phylogenetic approaches in the tribe Gaultherieae (Ericaceae). We test relationships between fruit colour and (a) biogeographic dispersal, (b) elevational and latitudinal species distributions and (c) rates of diversification.

    Location

    Global.

    Time period

    Recent to 30 million years ago.

    Major taxa studied

    The plant tribe Gaultherieae in the family Ericaceae (blueberries and relatives).

    Methods

    We estimated a new time‐calibrated phylogeny for Gaultherieae. Data on fruit colours and geographic distributions for each species were compiled from published sources and field observations. Using phylogenetic methods, we estimated major dispersal events across the tree and the most likely fruit colour associated with each dispersal event, and tested whether dispersal between major biogeographic regions was equally likely for different fruit colours, and whether dispersal distances were larger for certain colours. We then tested the relationships between fruit colours and geographic variables (latitude, elevation) and diversification rates.

    Results

    Large‐scale dispersal events were significantly associated with red‐fruited lineages, even though red‐fruited species were relatively uncommon. Further, different fruit colours were associated with different elevations and latitudes (e.g. red at lower elevations, violet at lower latitudes, white at higher elevations). Violet colour was related to increased diversification rates, leading to more violet‐fruited species globally.

    Main conclusions

    Overall, we show that different fruit colours can significantly impact the large‐scale dispersal, distribution and diversification of plant clades. Furthermore, the interplay between biogeography and fruit‐colour evolution seems to generate “taxon cycles” in fruit colour that may drive variation in fruit colour over macroevolutionary time‐scales.

     
    more » « less
  5. Abstract Aim

    Island biotas face an array of unique challenges under global change. Monitoring and research efforts, however, have been hindered by the large number of islands, their broad distribution and geographical isolation. Global citizen‐science initiatives have the potential to address these deficiencies. Here, we determine how the eBird citizen‐science programme is currently sampling island bird assemblages annually and how these patterns are developing over time.

    Location

    Global.

    Taxa

    Birds.

    Methods

    We compiled occurrence information of non‐marine bird species across the world's islands (n = 21,813) over an 18‐year period (2002–2019) from eBird. We estimated annual survey completeness and species richness across islands, which we examined in relation to six geographical and four climatic features.

    Results

    eBird contained bird occurrence information forca. 20% of the world's islands (n = 4,205) withca. 8% classified as well surveyed annually (n = 1,644). eBird participants tended to survey larger islands that were more distant from the mainland. These islands had lower proximity to other islands and contained a broader range of elevations. Temperature, precipitation and temperature seasonality were at intermediate levels. Precipitation seasonality was at low and intermediate levels. Islands located between 10 and 60° N latitude and 20 and 40° S latitude were overrepresented, and islands located in Southeast Asia were underrepresented. From 2002 to 2019, the number of islands surveyed annually increased byca. 96.4 islands/year. During this period, island size decreased, distance from mainland did not change, proximity to other islands increased and elevation range decreased.

    Main conclusions

    The eBird programme tends to survey larger islands containing intermediate climates that are more isolated from the mainland and other islands. These findings provide a framework to support the informed application of the eBird database in avian island biogeography. Our findings emphasize citizen science as an empirical resource to support long‐term ecological research, conservation and monitoring efforts across remote regions of the globe.

     
    more » « less