Translocation of cave fish (Poecilia mexicana) within and between natural habitats along a toxicity gradient
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Ecology of Freshwater Fish 2012 Ó 2012 John Wiley & Sons A/S
Printed in Malaysia All rights reserved
ECOLOGY OF
FRESHWATER FISH
Translocation of cave fish (Poecilia mexicana)
within and between natural habitats along a
toxicity gradient
Ingo Schlupp1, Timothy J. Colston2, Brandon L. Joachim1, Rüdiger Riesch3
1
Department of Biology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA
2
Biology Department, University of Mississippi, Box 1848, University, MS 38677, USA
3
Department of Biology, North Carolina State University, 127 David Clark Labs, Raleigh, NC 27695-7617, USA
Accepted for publication October 16, 2012
Abstract – During ecological speciation, diverging taxa have the potential to remain in close spatial proximity
(i.e., sympatry or micro-allopatry) theoretically allowing for continued contact and gene flow. In a system where
incipient speciation of populations of the Atlantic molly (Poecilia mexicana) appears to be driven by abiotic
factors, we investigated whether one of these factors, hydrogen sulphide (H2S) toxicity, also constitutes an
effective barrier to slow migration within and between habitats. We addressed this experimentally by
translocating individuals from high toxicity to lower toxicity within a toxic cave and by translocating individuals
from the toxic cave to a nontoxic surface habitat. Using a stepwise-backwards Cox regression, we found that
overall mortality was low, but statistically significant mortality occurred when individuals were transferred from
higher toxicity to lower toxicity. In addition, only males were negatively affected by being transferred from low
levels of toxicity to nontoxic, surface waters. This indicates that in addition to abiotic factors, other mechanisms,
like predation and sexual selection, must be important in maintaining population separation.
Key words: ecological speciation; divergence; habituation; acclimation; troglobite
mechanisms in detail likely also advances our under-
Introduction
standing of how sympatric speciation occurs.
While it has long been accepted that geographic Abiotic factors often play an important role in
isolation can lead to speciation (i.e., allopatric specia- maintaining population separation and divergence
tion; Mayr 1963; Coyne & Orr 2004), a number of (Tobler et al. 2006). However, these factors often
mechanisms, including sexual (Maan & Seehausen represent soft gradients, rather than sharp clines
2011) and natural selection (Schluter 1993; Riesch (i.e., abrupt demarcation with presence of a factor on
et al. 2011b), can lead to population divergence and one side and absolute absence of that factor on the
eventually to ecological speciation even in sympatry other), along which populations are positioned. It is
(Rundle & Nosil 2005). Once populations show signs important to understand to which degree these differ-
of phenotypic and genetic divergence, and are on an ent gradients contribute to divergence, and a sharper
evolutionary trajectory that could lead to speciation, cline is thought to lead to conditions under which
mechanisms must be in place to reduce the probabil- divergence can evolve easier (Nosil et al. 2009a,b).
ity of reticulation, or the collapse of the nascent spe- Classical work in botany, for example, has estab-
cies (Woehrer et al. 2012). Mechanisms responsible lished how important sharp clines in soil composition
for maintaining species separation were potentially can be in population divergence (Dickinson &
also important in generating divergence (but see Antonovics 1973; Antonovics & Thrall 1994). A
Coyne & Orr 2004), and thus studying these combination of sharp and soft gradients, on the other
Correspondence: I. Schlupp, Department of Biology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA. E-mail: schlupp@ou.edu
doi: 10.1111/eff.12017 1Schlupp et al. hand, along which organisms can potentially move selection, which would enable us to study the under- up and down, occur in a cluster of populations of the lying genomic architecture of divergence (Nosil Atlantic molly (Poecilia mexicana) from Tabasco, 2012). Mexico (Tobler & Plath 2011). Here, a population of Previous work on mechanisms isolating the cave Atlantic mollies has colonised a toxic cave, the and the surface populations has documented that sud- Cueva del Azufre (or Cueva de Villa Luz), that has den translocation of surface fish into nonfamiliar hab- been under study since its scientific discovery in the itat (i.e., toxic to nontoxic and vice versa) leads to 1960s (Gordon & Rosen 1962; Parzefall 2001). The high mortality (Tobler et al. 2009; Plath et al. 2010), Cueva del Azufre is divided into 13 different cham- while sudden translocation within toxic habitats (i.e., bers, with chamber XIII being the innermost chamber toxic surface to toxic cave and vice versa) yielded no (Gordon & Rosen 1962). Several springs in the cave measurable mortality (Tobler et al. 2009). Thus, (mainly in chamber X) release water that is extremely toxicity limits successful migration and promotes iso- rich in hydrogen sulphide, thus forming a toxicity lation between fish from nontoxic and toxic habitats. gradient within the cave that varies in levels of The proposed mechanism behind the high mortality hydrogen sulphide depending on the relative position is physiological incompatibility with the new condi- to the springs (Tobler et al. 2006). As the toxic water tions for either form (Tobler et al. 2009). Nonethe- flows downstream in the cave, it is oxygenated and, less, this result comes as somewhat of a surprise, as a result, becomes less toxic with greater distance because over the last couple of decades, experimental from the springs. The creek that flows through the populations of P. mexicana have successfully and cave eventually leaves the cave and becomes the repeatedly been established from toxic (surface and toxic El Azufre, a surface creek also containing cave) habitats in benign (i.e., nontoxic) laboratory hydrogen sulphide. While toxicity represents a some- environments after acclimation to nontoxic water. what soft gradient, the change from darkness within Why then was mortality in the field experiments so the cave to light at the mouth of the cave is abrupt. high? This could be due to the sudden exposure to The community of organisms inhabiting the waters either relatively high levels of hydrogen sulphide (for of the Cueva del Azufre and El Azufre is extremely fish from nontoxic waters) or relatively high levels of depauperate given its geographic location in the tro- oxygen (for fish from toxic waters) following translo- pics (Gordon & Rosen 1962). The Atlantic molly is cation (Tobler et al. 2009). the only fish species that has permanently colonised Thus, while previous translocation experiments the spring habitats within the cave (Tobler et al. have addressed how well individuals would fair after 2006; Riesch et al. 2009). Populations of P. mexicana rapid transport into a foreign environment, the more inhabiting the toxic cave are fundamentally different plausible scenario of slow and gradual acclimation from surface-living populations in almost every of individuals to a new habitat has so far not been aspect of their natural history (e.g., behaviour: Plath considered experimentally. As toxicity in the cave et al. 2004; morphology: Tobler et al. 2008a; life his- molly system represents a gradient, one can hypoth- tory: Riesch et al. 2010b), and using common-garden esise that slower, more gradual movement along the experiments, these differences have repeatedly been gradient would allow individuals a higher probability shown to have a strong heritable component (e.g., of survival when migrating from more toxic to less behaviour: Parzefall 2001; morphology: Tobler et al. toxic conditions. This question is also important 2008a; life history: Riesch et al. 2011a; Physiology: relative to the surprisingly strong genetic structuring Plath & Tobler 2010). Thus, the combined evidence within the toxic cave. While there is strong genetic indicates a system in which ongoing, incipient specia- structure even between chambers within the Cueva tion is occurring (Plath et al. 2007a; Tobler & Plath del Azfure, there is, nonetheless, evidence for low 2011). Clearly such early splitting events are labile levels of gene flow between different cave chambers. and vulnerable to collapse if conditions change (Wu On the other hand, we have so far found no evi- & Ting 2004; Hendry 2009; Nosil et al. 2009a,b; dence for any gene flow from migrants between the Bolnick 2011; Yeaman & Whitlock 2011; Woehrer toxic surface and toxic cave on one side and the et al. 2012), although so far we have no evidence for nontoxic surface habitats on the other side, further this happening in P. mexicana. In fact, we have corroborated by FST values that are usually above strong evidence indicating that population divergence 0.2 for any possible pairwise comparison (Plath is relatively stable because phenotypic and genetic et al. 2007a, 2010; Tobler et al. 2008a, 2009). For divergence has remained strong even if faced by example, Tobler et al. 2009 were able to demon- strong temporary disturbance due to natural catastro- strate that, based on microsatellite DNA, less than phes (like extreme flooding events; Plath et al. 2010). 10% first-generation migrants move from the inside This said, there are other outcomes possible, includ- of the Cueva del Azufre into the adjacent toxic ing stable divergence with limited gene flow and surface stream, while first-generation migrants within 2
Translocation of cave fish
these habitats (e.g., between different cave cham- and because seining is impossible due to the topogra-
bers) ranged anywhere from 5 to 35%. Interestingly, phy of the cave. Fishes were subsequently moved to
a study investigating the population genetic struc- individual containers (30.48 9 8.89 9 17.78 cm) (L
ture, following a millennium flood in 2007 (Plath 9 H 9 W) and placed in cave chambers that featured
et al. 2010), found slightly higher numbers of lower concentrations of H2S than the local area of
migrants within the cave immediately after the collection (i.e., chamber X fish were moved to cham-
event, pointing to a potential role of rare but cata- ber V; chamber V fish were moved to chamber II and
strophic events. What maintains population structur- chamber V fish moved to the surface habitat). As a
ing between (and within) the Cueva del Azufre and control, fishes from chamber V were captured and
the nontoxic surface habitats (Plath et al. 2007a, placed in individual containers within the same
2010; Tobler et al. 2008a)? Are individuals so well chamber. We aimed for an even sex ratio in the
adapted to the local conditions that dispersal even experimental fish, but were somewhat limited by the
within the cave is limited? fish available in the respective chambers (Table 1).
In this study, we addressed the following ques- For the experiment in which chamber V fish were
tions: how do fish fair if they are translocated along translocated to the surface habitat, we used a modi-
the toxicity gradient within the cave, where the other fied protocol. Fishes were collected as described,
environmental gradient (darkness) remains kept in two 19-litre coolers in their habitat-specific
unchanged? Furthermore, does acclimation to the water. This water was aerated for 4 h using portable
local conditions play a role when fish are transferred air pumps, which slowly removed hydrogen sul-
from the toxic cave to nontoxic surface waters? phide and oxygenized the water. After 4 h, we grad-
Finally, do the sexes respond differently to transloca- ually replaced the cave water with river water from
tions? To tackle these questions, we conducted three the nearby Río Oxolotán, a freshwater surface habi-
separate translocation experiments, all of which were tat. The next morning fish were then placed in indi-
designed to take individuals from higher toxicity to vidual containers in a surface habitat, Arroyo
lower toxicity. In the first experiment, we translocat- Bonita, a small tributary to the Río Oxolotán (both
ed fish from the very toxic chamber X to the less the Río Oxolotán and the Arroyo Bonita are natu-
toxic chamber V. In our second experiment, we rally populated by the surface form of P. mexicana).
moved individuals from chamber V to the even less Overnight mortality was low; during our overnight
toxic chamber II, and finally, in a third experiment, acclimation period of chamber V fish, only one male
we translocated fishes from chamber V to a nontoxic died.
surface habitat after acclimating them to nontoxic Previous studies have utilised large containers
water overnight. (buckets with holes drilled into them) with multiple
fish in the same container (Tobler et al. 2009). How-
ever, we chose to use smaller individual containers to
Materials and methods
minimise any stress that may be associated with
crowding. Additionally, small holes were drilled in
Study system
each container to allow for the circulation of water.
All experiments were conducted in January 2010 Each container contained one fish and was weighed
near Tapijulapa, Tabasco, Mexico. We selected fish down with small rocks that were gathered locally.
from habitats containing high hydrogen sulphide Containers were placed in a shallow area with low
concentrations (chamber X: 91.5 ± 32.3 lM), low flow to avoid having the containers washed away.
concentrations of hydrogen sulphide (chamber V: Due to the low oxygen concentrations in the Cueva
28.4 ± 15.3 lM) and very low concentrations of del Azufre, cavernicolous P. mexicana spend the
hydrogen sulphide (chamber II: 24.0 ± 21.6 lM) majority of their time at the water’s surface perform-
(Tobler et al. 2006). Additionally, fish were translo- ing aquatic surface respiration (ASR) to exploit
cated to a nontoxic surface stream, the Arroyo increased oxygen levels (Tobler et al. 2006). There-
Bonita (17o25′37.42″N, 92o45′6.98″W). The Arroyo fore, we did not fully submerge our containers to
Bonita is approximately 2 km upstream from where avoid mortality that could be attributed to behaviour-
the outflow of the Cueva del Azufre connects to the al limitations. Once all fish were placed in individual
Río Oxolotán, and does not contain hydrogen sul- containers, we allowed 1 h for acclimatisation and
phide (Tobler et al. 2008a). subsequently checked the condition of the fish in
each habitat (see Table 1). At the termination of each
experiment (after 24 h), fish were removed from
Local adaptation and natural selection
containers, sacrificed and preserved in 5% formalde-
Fish were collected by hand with small dip nets in hyde to avoid inadvertent mixing of populations. All
each cave chamber to minimise stress from handling individuals used in the experiment were adult. For
3Schlupp et al.
Table 1. Detail of the translocation experiments.
(a)
Sample size Mortality
Experiment Date From → to (males/females) (males/females)
1a 090111 X →V 7/13 2/2
1b 100111 X →V 9/11 2/1
2a 090111 V → II 9/11 0/0
2b 100111 V → II 10/10 0/0
3 120111 V →V 10/10 0/0
4 130111 V → Bonita 21/19 6/0
logistical reasons, we were unable to conduct a study
that would have measured mortality over a longer
term. Similarly, we were unable to conduct a control
experiment within chamber X. (b)
Statistical analysis
We used a stepwise-backwards Cox regression based
on likelihood ratios to analyse individual survival of
P. mexicana as implemented in IBM® SPSS® Statis-
tics 19.0.0 (IBM Corporation). In the original model,
‘treatment’ (PSX-to-PSV, PSV-to-PSV, PSV-to-PSII
and PSV-to-AB), ‘sex’ (male vs. female) and the
interaction of ‘treatment-by-sex’ were included as
covariates.
Results Fig. 1. Survival plot indicating cumulative survival (%) over time
When analysing the survival of cave-dwelling for (a) fish translocated between from chamber X to chamber V
within the toxic Cueva del Azufre and (b) fish translocated from
P. mexicana in different habitats, the covariate ‘sex’ the inside of the toxic Cueva del Azufre (chamber V) to a
(P = 0.868) was removed from the final Cox regres- nontoxic surface stream (Arroyo Bonita).
sion model during the stepwise-backwards approach.
Only the covariates ‘treatment’ (B = 0.84,
SE = 0.39, Wald = 4.69, d.f. = 1, P = 0.03) and the gence and ultimately ecological speciation. Sharp
interaction term ‘treatment-by-sex’ (B = 0.58, clines, like the difference between dark and light in
SE = 0.29, Wald = 3.91, d.f. = 1, P = 0.048) were the cave molly system, are much more likely to aid
retained as statistically significant in the final model population separation than soft gradients (Nosil et al.
( 2 log likelihood = 127.42). 2009a,b), as exemplified by the hydrogen sulphide
Overall we detected very low mortality across gradient known for the cave molly within the Cueva
treatments. No mortality was uncovered in two treat- del Azufre. In our particular system, we examined
ments (PSV-to-PSV and PSV-to-PSII), while some how differences in hydrogen sulphide toxicity affect
mortality occurred in the other two treatments (PSX- the survival of immigrants, and therefore population
to-PSV and PSV-to-AB, Fig. 1; significant ‘treat- structuring, between populations within the Cueva
ment’ effect). Furthermore, while males and females del Azufre. Previous research indicated that abrupt
suffered roughly similar mortality rates when trans- changes in water conditions (i.e., toxic to nontoxic
ferred from highly toxic waters (PSX) to low levels and vice versa) lead to very high mortality in translo-
of toxicity (PSV), only males were negatively cated fishes, but that translocation between chamber
affected by being transferred from low levels of II and the El Azufre (i.e., toxic cave and toxic sur-
toxicity (PSV) to nontoxic waters (AB, Fig. 1; face) resulted in no measurable mortality (Tobler
significant ‘treatment-by-sex’ effect). et al. 2009). In the experiment presented here, in
which we tested for survivorship during gradual
migration from highly toxic to lesser toxic microhabi-
Discussion
tats (i.e., cave chambers) within the cave, we found
How animals can move along relevant environmental low levels of mortality in two of four treatments. This
gradients is important for our understanding of diver- indicates that differences in toxicity found within the
4Translocation of cave fish
cave do not fully explain the genetic structure uncov- induced translocation during a religious ceremony, in
ered by previous studies (Plath et al. 2007a, 2010; which cave fishes are poisoned and immobilized
Tobler et al. 2008a). Clearly, factors other than the resulting in passive downstream drifting (Tobler et al.
toxicity gradient must play a role here in limiting 2011a), is not likely to lead to successful gene flow
between-chamber movement, and we can only specu- due to the high mortality induced by rapid transloca-
late that they could include sexual selection, preda- tion between extreme and benign environments (To-
tion and age-specific mortality. Furthermore, we bler et al. 2009). Under the scenario that we
found that translocation from a toxic cave habitat to a investigated here that envisions gradual movement
nontoxic surface habitat results in relatively low mor- along a gradient allowing for potential acclimatisation,
tality if the water is slowly detoxified and fish have previously described additional selective forces acting
time to adjust to the new conditions. against migrants (e.g., predation: Tobler 2009; Riesch
Interestingly, males turned out to be significantly et al. 2010a; sexual selection: Tobler et al. 2008b) are
more likely to die than females, when translocated likely to contribute more to reproductive isolation than
from toxic waters within the cave to a nontoxic previously assumed (Tobler 2009). Finally, the higher
surface water habitat. Sex-specific responses to physi- survival of females, nonetheless, raises the interesting
ological stress are widespread among animal taxa (e. possibility of sex-specific dispersal that should be
g., insects: Freitak et al. 2012; rats: Sterrenburg et al. investigated further in future studies.
2011; humans: Verma et al. 2011), and even though
this depends on the taxa under investigation and the
stressors involved, males often seem to be more sen- Acknowledgements
sitive to stressful conditions (Freitak et al. 2012; but We are very grateful to the people and authorities of Tapijula-
see Riesch et al. 2011b). In our system, it is not clear pa and the Federal authorities of Mexico for granting permits.
what exactly is causing this. Nonetheless, our finding Francisco García de León and Lenin Arias-Rodriguez helped
is congruent with data from previous field experi- logistically and with fieldwork. Funding for this project came
ments in this system in which males usually also per- from NSF (DEB-0743406). This work was conducted under
formed worse than females (Plath et al. 2007a,b). University of Oklahoma IACUC R09-030. We are also thank-
ful to the reviewers who helped greatly to improve the manu-
Likely males are physiologically less capable of buf-
script. IS gratefully acknowledges support from the Alexander
fering adverse conditions than females, potentially
von Humboldt Foundation.
due to the lower body condition of cave molly males
exhibited within the Cueva del Azufre, indicating the
males might be more energy limited than females References
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