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\begin{document}

\title{``Life histories'' is a more appropriate term than ``ecotypes'' to
describe ocean- and stream-maturing Pacific lamprey Entosphenus
tridentatus}



\author[1,2]{Benjamin Clemens}%
\author[3]{Carl Schreck}%
\affil[1]{Oregon State University}%
\affil[2]{Oregon Department of Fish and Wildlife}%
\affil[3]{US Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, USGS}%


\vspace{-1em}



  
  \date{May 19, 2024}


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\selectlanguage{english}
\begin{abstract}
The scientific literature includes a plethora of terms to denote
within-species phenotypic diversity (e.g., morphotypes; ecotypes;
ecomorphotypes; ecophenotypes; polymorphisms; and life histories). Here
we discuss a particular situation in which different terms (ecotypes and
life histories) have been used to describe the same within-species
diversity of adult Pacific lamprey Entosphenus tridentatus, note an
important challenge in using ``ecotypes'', and conclude with a
recommendation to use ``life histories'' to describe the ocean- and
stream-maturing forms of Pacific lamprey.%
\end{abstract}%



\sloppy


\textbf{Abstract}

The scientific literature includes a plethora of terms to denote
within-species phenotypic diversity (e.g., morphotypes; ecotypes;
ecomorphotypes; ecophenotypes; polymorphisms; and life histories). Here
we discuss a particular situation in which different terms
(ecotypes\emph{and} life histories) have been used to describe the same
within-species diversity of adult Pacific lamprey \emph{Entosphenus
tridentatus} , note an important challenge in using ``ecotypes'', and
conclude with a recommendation to use ``life histories'' to describe the
ocean- and stream-maturing forms of Pacific lamprey.

The scientific literature includes a plethora of terms to denote
within-species phenotypic diversity. These include morphotypes (Lessios
and Weinberg 1994; Chavarie et al. 2013; Collyer et al. 2015); ecotypes
(Gregor 1944; Arostegui et al. 2018; Cruz-Font 2019); ecomorphotypes
(Baker et al. 1998; Segura-Trujillo et al. 2018; Kloh et al. 2019);
ecophenotypes (Sch\selectlanguage{ngerman}önborn and Peschke 1988; Sorensen and Lindberg 1991;
Pro\selectlanguage{polish}ć\selectlanguage{english}k\selectlanguage{ngerman}ów et al. 2018); polymorphisms (Skúlason and Smith 1995; Skúlason
et al. 2019; Jamie and Meier 2020); and life histories (Stearns 1989;
Winemiller and Rose 1992). Several of these terms have common roots, and
are often used inter-changeably or in combination (e.g., Baker et al.
1998; Chavarie et al. 2013; Brannon et al. 2004; Wood et al. 2008;
Palacios et al. 2012). The use of these terms may suggest perceived or
actual novelty, a unique take on biological phenomena, or an attempt to
follow precedents. Here we discuss a particular situation in which
different terms (ecotypes \emph{and} life histories) have been used to
describe the same within-species diversity of adult Pacific
lamprey\emph{Entosphenus tridentatus} , note an important challenge in
using ``ecotypes'', and conclude with a recommendation to use ``life
histories'' to describe the ocean- and stream-maturing forms of Pacific
lamprey.

The Pacific lamprey is a jawless and boneless anadromous fish from a
primitive taxon (Petromyzontiformes; Docker et al. 2015; Potter et al.
2015). Parker et al. (2019) genotyped Pacific lamprey at adaptive and
neutral single nucleotide polymorphisms and measured the proportional
egg mass of females to identify a genetic basis for phenotypic variation
in ocean- and stream-maturing lamprey. Their research offers an
important contribution to the understanding of evolution and ecology in
general, and of Pacific lamprey in particular. The results of Parker et
al. support the conclusions of Clemens et al. (2013), who initially
identified this same diversity from comprehensive phenotypic
characteristics that included morphology and physiology of proportional
body and organ sizes and dimensions, and use of histology to identify
stages of gonadal development. Rather than ``ecotypes'', Clemens et al.
described the ocean- and stream-maturing forms as ``life histories''.

We offer three inter-related reasons to argue that, given the present
scientific knowledge regarding the Pacific lamprey, ``life histories''
is a more appropriate (i.e. conservative) term than ``ecotypes'' to
describe within-species variation of maturation schedules:

\begin{enumerate}
\tightlist
\item
  Current information is insufficient to conclude that the ocean- and
  stream-maturing forms are genetically distinguishable phenotypes
  occupying different habitats, rather than life histories that display
  life history trade-offs. Ecotype has been defined as ``the product
  arising as a result of the genotypical response of an ecospecies to a
  particular habitat'' (Turesson 1922, cited in Gregor 1944), and has
  been used to describe the use of different niches by different forms
  of the same species (e.g., benthic and limnetic forms of the
  threespine stickleback \emph{Gasterosteus aculeatus} ; Baker et al.
  2005, and the forms of marine snail \emph{Littorina saxatilis} that
  have adapted to the action of waves or predation by crabs; Westram et
  al. 2014). In lampreys, the term ecotypes has been synonymized with
  closely-related species pairs, where one species is parasitic as a
  juvenile, whereas the other species does not have a juvenile feeding
  stage (Rougemont et al. 2017). Docker and Potter (2019) furthered this
  argument with the description of two situations where lamprey ecotypes
  could either be partially or fully reproductively isolated. It is not
  known whether ocean- and stream-maturing Pacific lamprey occupy
  different niches at any point in their life cycle, and they co-occur
  during the freshwater spawning migration. Further, assessment of the
  neutral alleles of ocean- and stream-maturing Pacific lamprey suggests
  one panmictic population with no ecotypic differentiation (i.e., no
  reproductive isolation; Parker et al. 2019). We appreciate that Parker
  et al. raise the concept of ecotypes when referring to the
  reproductive variation of ocean- and stream-maturing Pacific lamprey
  because this has important evolutionary and management implications.
  However, to conclude that environmental selection was responsible for
  the evolutionary divergence of ecotypes from a common ancestor would
  require evidence that these ecotypes encountered some degree of
  reproductive isolation. Knowledge of the different habitats occupied
  by each phenotype could greatly enhance monitoring and conservation
  practices for Pacific lamprey.
\item
  The names of the phenotypes were chosen by Clemens et al. (2013) to
  place understanding of them within the template of what is known about
  other, more well-studied species. The terms ocean- and
  stream-maturing, and life histories were used by Clemens et al. to
  place the morphological and physiological information on Pacific
  lamprey from their study into the context of the extensive
  evolutionary and ecological literature on Pacific
  salmon\emph{Oncorhynchus} spp. (Healey 1991; Hendry and Stearns 2004;
  Quinn 2005), particularly steelhead \emph{O. mykiss} (Busby 1996;
  Brannon et al. 2004; Quinn 2005), as a template to advance
  understanding of Pacific lamprey. Pacific salmon are sympatric with
  Pacific lamprey, and steelhead (like Pacific lamprey) spawn in the
  spring (Quinn 2005; Clemens et al. 2013).
\item
  ``Life history'' connotes demographic diversity of phenotypes, which
  pertains to correlations and trade-offs among organismal
  characteristics of mortality, growth, fecundity, age-at-maturation,
  and body size (Stearns 1989; Winemiller and Rose 1992; Ricklefs and
  Wikelski 2002). Clemens et al. used the term ``life history'' to place
  the within-species diversity they identified for Pacific lamprey into
  the well-established life history paradigm of Winemiller and Rose
  (1992). Clemens et al. furthermore used the scheme of Winemiller and
  Rose to conclude that Pacific lamprey, as a species, is a ``periodic''
  life history strategist.
\end{enumerate}

It will be important to identify the habitat use and extent of
distribution of ocean- and stream-maturing life histories of Pacific
lamprey. If ocean-maturing lamprey spawn in the same year that they
enter freshwater, then one would predict life history differences
relative to stream-maturing Pacific lamprey. For example, less time
holding in fresh water prior to spawning could yield higher adult
survival and fecundity for ocean-maturing lamprey relative to
stream-maturing lamprey. This is because less time holding in freshwater
before spawning could translate to less exposure to predation or other
mortality sources, and more energy that could be used for generating a
higher fecundity rather than being used to prolong life prior to
spawning. We conclude that ``ecotype'' suggests a fundamental difference
in geographic or habitat distribution between ocean- and stream-maturing
Pacific lamprey that has not been demonstrated. However, ``life
histories'' more accurately describes the diversity of schedule over
which conspecifics mature and reproduce.

\textbf{Data accessibility statement}

No data are associated with this essay.

\textbf{Competing interests}

The authors have no competing interests.

\textbf{Author contributions}

Ben Clemens conceived the idea for this essay and led the writing and
editing. Carl Schreck contributed to the ideas, writing, and editing.

\textbf{Funding information}

Ben Clemens was funded by the Oregon Department of Fish and Wildlife.
Carl Schreck was funded by the Department of Fisheries and Wildlife at
Oregon State University.

\textbf{Acknowledgments}

We would like to thank Tom Stahl, Marc Johnson, and David Noakes for
providing reviews and comments that improved an early draft of this
manuscript.

\textbf{References}

Arostegui, M. C., T. P. Quinn, L. W. Seeb, J. E. Seeb, G. J. McKinney.
2018. Retention of a chromosomal inversion from an anadromous ancestor
provides the genetic basis for alternative freshwater ecotypes in
rainbow trout. Molecular Ecology. 28: 1412 -- 1427.

Baker, J. A., W. A. Cresko, S. A. Foster, and D. C. Heins. 2005.
Life-history differentiation of benthic and limnetic ecotypes in a
polytypic population of threespine stickleback (\emph{Gasterosteus
aculeatus} ). Evolutionary Ecology Research. 7: 121 -- 131.

Baker, J. A., S. A. Foster, D. C. Heins, M. A Bell, and R. W. King.
1998. Variation in female life-history traits among Alaskan populations
of the threespine stickleback, \emph{Gasterosteus aculeatus} L. (Pisces:
Gasterosteidae). Biological Journal of the Linnean Society. 63: 141 --
159.

Brannon, E. L., M. S. Powell, T. P. Quinn, and A. Talbot. 2004.
Population structure of Columbia River Basin Chinook salmon and
steelhead trout. Reviews in Fisheries Science. 12: 99 -- 232.

Busby, P. J., T. C. Wainwright, G. J. Bryant, L. J. Lierheimer, R. S.
Waples, F. W. Waknitz, and I. V. Lagomarsino. 1996. Status review of
west coast steelhead from Washington, Idaho, Oregon, and California.
National Oceanographic and Atmospheric Administration Tech. Memo.
NMFS-NWFSC-27.

Chavarie, L., K. L. Howland, and W. M. Tonn. 2013. Sympatric
polymorphism in Lake Trout: The coexistence of multiple shallow-water
morphotypes in Great Bear Lake. Transactions of the American Fisheries
Society. 142: 814 -- 823.

Clemens, B. J., van de Wetering, S., Sower, S. A., and Schreck, C. B.
2013. Maturation characteristics and life\selectlanguage{english}-history strategies of the
Pacific lamprey, \emph{Entosphenus tridentatus} . Canadian Journal of
Zoology, 91: 775 -- 788.

Collyer, M. L., M. E. Hall, M. D. Smith, and C. W. Hoagstrom. 2015.
Habitat-morphotype associations of Pecos pupfish (\emph{Cyprinodon
pecosensis} ) in isolated habitat complexes. Copeia, 2015(1): 181 --
199.

Cruz-Font, L., B. J. Shuter, P. J. Blanchfield, C. K. Minns, and M. D.
Rennie. 2019. Life at the top: Lake ecotype influences the foraging
pattern, metabolic costs and life history of an apex fish predator.
Journal of Animal Ecology. 88: 702 -- 716.

Docker, M. F., J. Hume, and B. J. Clemens. 2015. Introduction: A surfeit
of lampreys. Pages 1 -- 34 In: M. F. Docker (editor), Lampreys: biology,
conservation and control, Volume 1. Springer, Fish and Fisheries
Monograph Series, New York.

Docker, M.F., and I. C. Potter. 2019. Life history evolution in
lampreys: Alternative migratory and feedings types, in: Docker, M.F.
(Ed.), Lampreys: biology, conservation and control. Vol. 2. Fish and
Fisheries Series, Vol. 38. Springer, Dordrecht, The Netherlands, pp. 287
-- 410.

Gregor, J. W. 1944. The ecotype. Biological Reviews. 19: 20 -- 30.

Healey, M.C. 1991. Life history of Chinook salmon (\emph{Oncorhynchus
tshawytscha} ). In: Groot, C.; Margolis, L., eds. Pacific salmon life
histories. Vancouver, BC: University of British Columbia Press: 311-393.

Hendry, A. P., and S.C. Stearns. 2004. Evolution illuminated: salmon and
their relatives. Oxford University Press, New York.

Kloh, J. S., C. C. Figueredo, and P. C. Eterovick. 2019. How close is
microhabitat and diet association in aquatic ecomorphotypes? A test with
tadpoles of syntopic species. Hydrobiologia. 828: 271 -- 285.

Lessios, H. A., and J. R. Weinberg. 1994. Genetic and morphological
divergence among morphotypes of the isopod \emph{Excirolana} on the two
sides of the isthmus of Panama. Evolution. 48: 530 -- 548.

Palacios, M. G., A. M. Sparkman, and A. M. Bronikowski. 2012.
Corticosterone and pace of life in two life-history ecotypes of the
garter snake \emph{Thamnophis elegans} . General and Comparative
Endocrinology. 175: 443 -- 448.

Parker, K., J. E. Hess, S. R. Narum, and A. P. Kinziger. 2019. Evidence
for the genetic basis and epistatic interactions underlying ocean\selectlanguage{english}- and
river\selectlanguage{english}-maturing ecotypes of Pacific Lamprey (Entosphenus tridentatus)
returning to the Klamath River, California. Molecular Ecology. 28: 3171
-- 3185.

Potter, I. C., H. S. Gill, C. B. Renaud, and D. Haoucher. 2015. The
taxonomy, phylogeny, and distribution of lampreys. Pages 35 -- 74 In: M.
F. Docker (editor), Lampreys: biology, conservation and control, Volume
1. Springer, Fish and Fisheries Monograph Series, New York.

Pro\selectlanguage{polish}ć\selectlanguage{english}k\selectlanguage{ngerman}ów, M., J. Pro\selectlanguage{polish}ć\selectlanguage{english}k\selectlanguage{ngerman}ów, P. B\selectlanguage{polish}ł\selectlanguage{english}a\selectlanguage{polish}ż\selectlanguage{english}ej, P. Mackiewicz. 2018. The influence
of habitat preferences on shell morphology in ecophenotypes
of\emph{Trochulus hispidus} complex. Science of The Total Environment.
630:1036-1043

Quinn, T. P. 2005. The behavior and ecology of Pacific salmon and trout.
University of Washington Press, Seattle.

Ricklefs, R. E., and M. Wikelski. 2002. The physiology/life-history
nexus. Trends in Ecology and Evolution. 17: 462 -- 468.

Rougemont, Q., P.-A. Gagnaire, C. Perrier, C. Genthon, A.-L. Besnard, S.
Launey, and G. Evanno. 2017. Inferring the demographic history
underlying parallel genomic divergence among pairs of parasitic and
nonparasitic lamprey ecotypes. Molecular Ecology. 26: 142 -- 162.

Sch\selectlanguage{ngerman}önborn, W., and T. Peschke. 1988. Biometric studies on species,
races, ecophenotypes and individual variations of soil-inhabiting
Testacea (Protozoa, Rhizopoda), including \emph{Trigonopyxis minuta}nsp.
and \emph{Corythion asperulum} nsp. Archiv für Protistenkunde. 136:
345-363.

Segura-Trujillo, C. A., M. R. Willig, and S. T. Álvarez-Castañeda. 2018.
Correspondence between ecomorphotype and use of arthropod resources by
bats of the genus \emph{Myotis} . Journal of Mammalogy. 99: 659 -- 667.

Skúlason, S., and T. B. Smith. 1995. Resource polymorphisms in
vertebrates. 10: 366 -- 370.

Skúlason, S., K. J. Parsons, Richard Svanbäck , K. Räsänen, M. M.
Ferguson, C. E. Adams, P.-A. Amundsen, P. Bartels, C. W. Bean, J. W.
Boughman, G. Englund, J. Guðbrandsson, O. E. Hooker, A. G. Hudson, K. K.
Kahilainen, R. Knudsen, B. K. Kristjánsson, C. A-L. Leblanc, Z. Jónsson,
G. Öhlund, C. Smith, and S. S. Snorrason. 2019. A way forward with eco
evo devo: an extended theory of resource polymorphism with postglacial
fishes as model systems. Biological Reviews. 94: 1786 -- 1808.

Sorensen, F.E., and D.R. Lindberg. 1991. Preferential predation by
American black oystercatchers on transitional ecophenotypes of the
limpet \emph{Lottia pelta} (Rathke). Journal of Experimental Marine
Biology and Ecology. 154: 123-136.

Stearns, S. C. 1989. Trade-offs in life-history evolution. Functional
Ecology. 3: 259 --268.

Westram, A. M., J. Galindo, M. Alm Rosenblad, J. W. Grahame, M. Panova,
and R. K. Butlin. 2014. Do the same genes underlie parallel phenotypic
divergence in different \emph{Littorina saxatilis} populations?
Molecular Ecology. 23: 4603 -- 4616.

Winemiller, K.O., and K. A. Rose. 1992. Patterns of life-history
diversification in North American fishes: implications for population
regulation. Canadian Journal of Fisheries and Aquatic Sciences. 49: 2196
-- 2218.

Wood, C. C., J. W. Bickham, R. J. Nelson, C. J. Foote, and J. C. Patton.
2008. Recurrent evolution of life history ecotypes in sockeye salmon:
implications for conservation and future evolution. Evolutionary
Applications. 1: 207 -- 221.

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