Can You Deternmine An Animals Sex Based On Temperature

• Journal List
• PLoS One
• PMC2481392

PLoS 1. 2008; three(7): e2837.

Temperature-Dependent Sex Determination in Fish Revisited: Prevalence, a Single Sexual activity Ratio Response Blueprint, and Possible Effects of Climate Change

Natalia Ospina-Álvarez

Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), Barcelona, Spain,

Francesc Piferrer

Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), Barcelona, Espana,

Jerome Chave, Editor

Received 2008 Mar 5; Accustomed 2008 Jul nine.

Supplementary Materials

Table S1: Temperature-Dependent Sexual activity Determination in Fish. Prevalence, Being of a Single Sex Ratio Response Pattern, and Possible Effects of Climatic change.

(0.35 MB DOC)

GUID: 78A2E0DC-9F7E-4F4B-8F63-A958A3556569

Abstract

Background

In gonochoristic vertebrates, sexual activity decision mechanisms tin be classified as genotypic (GSD) or temperature-dependent (TSD). Some cases of TSD in fish take been questioned, but the prevalent view is that TSD is very common in this grouping of animals, with three dissimilar response patterns to temperature.

Methodology/Principal Findings

We analyzed field and laboratory data for the 59 fish species where TSD has been explicitly or implicitly claimed and then far. For each species, nosotros compiled data on the presence or absenteeism of sex chromosomes and adamant if the sex ratio response was obtained inside temperatures that the species experiences in the wild. If then, we studied whether this response was statistically pregnant. We found show that many cases of observed sexual practice ratio shifts in response to temperature reveal thermal alterations of an otherwise predominately GSD mechanism rather than the presence of TSD. We also bear witness that in those fish species that really accept TSD, sex ratio response to increasing temperatures invariably results in highly male-biased sexual practice ratios, and that even small changes of just 1–2°C tin can significantly alter the sexual activity ratio from 1∶i (males∶females) up to 3∶i in both freshwater and marine species.

Conclusions/Significance

We demonstrate that TSD in fish is far less widespread than currently believed, suggesting that TSD is conspicuously the exception in fish sex determination. Further, species with TSD exhibit only i general sex ratio response blueprint to temperature. All the same, the viability of some fish populations with TSD tin be compromised through alterations in their sex ratios every bit a response to temperature fluctuations of the magnitude predicted past climatic change.

Introduction

Sex decision mechanisms produce the sex ratio, a primal demographic parameter crucial for population viability. In gonochoristic vertebrates, sexual activity determining mechanisms tin broadly be classified every bit genotypic (GSD) or temperature-dependent (TSD) [i], [2]. In species with TSD, at that place are no consistent genetic differences between sexes. The earliest ontogenetic difference between sexes is an environmental one because the ambient temperature during sensitive periods of early on evolution irreversibly determines phenotypic sex and, therefore, the sexual activity ratio [1], [2]. Thus, species with TSD have been proposed to exist reliable indicators of the biological impact of global warming, since temperature-induced sex ratio shifts constitute a direct fitness response to thermal fluctuation [3].

So far, predicted effects of climate modify on fish populations include distribution shifts [4], alterations in developmental fourth dimension and larval dispersal [5], decrements in aerobic performance [half-dozen], and mismatches in species interactions [7]. Climate alter effects on the sex ratio accept already been inferred for some ocean turtles with TSD [viii], [9], but are lacking for fish. Thus, knowledge of the extent to which temperature affects sexual practice ratios is relevant in order to estimate potential threats of ascension temperatures on fish populations. Further, knowing the prevalence of TSD is essential for the correct theoretical and empirical study of the development of sex determining mechanisms [two], because otherwise inferences on the distribution and prevalence of a particular type of mechanism may be biased [x].

In fish, the start evidence of TSD was obtained in field and laboratory studies carried out in the Atlantic silverside, Menidia menidia (F. Atherinopsidae) [11]. Since then, TSD has been claimed in 59 different species (33 of them of the genus Apistogramma, F. Cichlidae, and all included in the same study) belonging to xiii families representative of many types of fishes (run across Tabular array S1 in the Supplementary Materials). Fish with TSD accept readily been grouped according to three patterns of sex ratio response to environmental temperature [12]–[16]: one, more males at high temperature; 2, more males at low temperature; and iii more than males at extreme (high and low) temperatures (Fig. 1). However, a critical examination of sex ratio produced in response to temperature in fish has never been carried out. Based on all the available data on TSD in fish, information technology has been reported that 53–55 (including the 33 species of the genus Apistogramma), two–4 and ii of these species follow patterns one, 2 and 3, respectively (Tabular array 1). Annotation that what here are referred to as patterns ane and 2 of fish essentially corresponds to what in reptiles are referred to as patterns Ib and Ia, respectively. However, pattern iii of fish is non equivalent to pattern II of reptiles (female person-biased sex ratios at depression and high temperatures and male person-biased sex ratios at intermediate temperatures) just it could be considered an changed of it.

Patterns of temperature-dependent sex activity determination (TSD) in fish that had been recognized to appointment.

They are defined according to the sexual activity ratio produced as a function of temperature during the thermosensitive catamenia. A, Pattern 1, low temperatures produce female-biased sex ratios and loftier temperatures produce male-biased sex ratios. B, Design 2, depression temperatures produce male person-biased sexual practice ratios and high temperatures produce female-biased sex ratios. C, Design 3, male-biased sex ratios are produced at low and high temperatures, while balanced sex ratios are produced at intermediate temperatures. In some cases, the response may be partial (dashed line in A). The present written report demonstrates that fish species with TSD only showroom pattern one.

Table i

Patterns of temperature-dependent sex determination in gonochoristic fish.

		Criteria used hither			Confirmation by statistical analyses
SPECIES	Pattern of TSD previously assigned*	Prove for the presence of sexual practice chromosomes [Reference]	Sex activity ratio shift within the RTD (see Suppl. Tabular array one)	Diagnosis	Lineal regression/F-test							New pattern of TSD proposed here*
					n	Intercept	Slope	rtwo	F	DFn/DFd	P
Carassius auratus	(one)	Yes [49]	No	GSD+TE	-	-	-	-	-	-	-	0
Carassius carassius	i	Yes [15]	No	GSD+TE	-	-	-	-	-	-	-	0
Danio rerio	(1)	Yes [38]	No	GSD+TE	-	-	-	-	-	-	-	0
Gnathopogon caerulescens	1	Yes [50]	Yeah	GSD+TE	-	-	-	-	-	-	-	0
Misgurnus anguillicaudatus	1	Aye [51]	Yes	GSD+TE	-	-	-	-	-	-	-	0
Ictalurus punctatus	two	Yes [52]	No	GSD+TE	-	-	-	-	-	-	-	0
Hoplosternum littorale	i	No	Yep	TSD	sixteen	two.53	2.26	0.40	9.30	1/14	0.009	one
Oncorhynchus nerka	2	Yes [53]	No	GSD+TE	-	-	-	-	-	-	-	0
Menidia menidia	i	No	Aye	TSD	ten	113.79	−995.21	−0.90	lxx.21	1/8	<0.0001	1
Menidia peninsulae	1	No	Yeah	TSD	xx	−27.81	2.74	0.58	24.61	1/18	0.0001	ane
Odontesthes argentinensis	one	No	Yeah	TSD	9	−55.62	3.91	0.67	14.42	i/seven	0.0067	i
Odontesthes bonariensis	one	No	Yes	TSD	vi	−182.40	9.39	0.98	242.xc	1/4	<0.0001	1
Odontesthes hatcheri	ane	No	No	GSD+TE	-	-	-	-	-	-	-	0
Oryzias latipes	(one)	Yes [54]	No	GSD+TE	-	-	-	-	-	-	-	0
Limia melanogaster	1	No	Aye	TSD	9	−22.15	2.lx	0.69	xv.29	one/seven	0.0058	ane
Poeciliopsis lucida	1	No	Aye	TSD	21	−139.fifty	vii.21	0.76	threescore.91	ane/19	<0.0001	1
Poecilia sphenops	(1)	Yep [55]	Yes	GSD+TE	-	-	-	-	-	-	-	0
Sebastes schlegeli	1	No	No	GSD+TE	-	-	-	-	-	-	-	0
Dicentrarchus labrax	1/2	No	No	GSD+TE	-	-	-	-	-	-	-	0
Apistogramma spp. (33 spp.) †	1×33	No	Aye	TSD	93	−75.93	4.78	0.75	283.60	1/91	<0.0001	ane×33
Oreochromis aureus	one	Yep [56]	Yes	GSD+TE	-	-	-	-	-	-	-	0
Oreochromis niloticus	ane/2	Yeah [57]	Yes	GSD+TE	-	-	-	-	-	-	-	0
Oreochromis mosambicus	1	Aye [58]	Yes	GSD+TE	-	-	-	-	-	-	-	0
Paralichthys olivaceus	three	Yes [59]	Yes	GSD+TE	-	-	-	-	-	-	-	0
Paralichthys lethostigma	3	No	No	GSD+TE	-	-	-	-	-	-	-	0
Pseudopleuronectes yokohamae	ane	Yes [60]	No	GSD+TE	-	-	-	-	-	-	-	0
Verasper moseri	1	No	No	GSD+TE	-	-	-	-	-	-	-	0

GSD and TSD can be regarded every bit two discrete processes that give rise to a continuous blueprint of sex conclusion mechanisms [ii], or as two ends of a continuum [17]. In whatsoever case, the presence of TSD in a given species is not incompatible with the existence of genotype x environment interactions, which are mutual in fish, including Menidia [xv], [18], [nineteen]. Even so, also often assignment of TSD in many fish species has proceeded regardless of prove such as the presence of sexual activity chromosomes, which is strongly indicative of GSD [1], [2], [15]. Further, the Atlantic silversides (Menidia menidia and G. peninsulae) are the only fish species in which the existence of TSD has been demonstrated in the wild; in all other species, information were obtained from laboratory experiments [16]. Thus, evidence to support the presence of TSD has been obtained in many cases using temperatures in the laboratory that the species will rarely feel in nature. It has been pointed out that observed sex ratio shifts under these circumstances might be the consequence of thermal effects on GSD (GSD+TE) rather than proof of the presence of TSD [2], [xvi]. Thus, in that location is business regarding the actual prevalence of TSD in fish. In particular, to discern true cases of TSD from GSD+TE [16]. Nevertheless, the beingness of TSD in fish is now widely accepted, assumed to exist widespread and expected to exist found in more than species as new studies get bachelor [ten], [12].

The objective of this written report was to appraise the prevalence of TSD in fish past taking the species where this type of sex determining mechanism has been claimed and applying a series of proposed criteria to discern true cases of TSD from cases of GSD+TE. These included checking for the presence of sex chromosomes and determining whether the temperature used to arm-twist a change in sex activity ratios was ecologically relevant, i.e., a temperature that the species ordinarily experiences in nature during the thermosensitive period. We found that TSD is far less widespread that currently idea. We also found that species who actually take TSD exhibit just one single response pattern, not three, producing highly male-biased sex activity ratios in response to fifty-fifty small increases in temperature. Thus, in one hand, by defining the species that actually accept TSD, this report contributes to our understanding of the evolution of sex activity determining mechanisms. On the other hand, it reports previously unaccounted possible furnishings of global warming on fish sexual practice ratios.

Materials and Methods

Species selection

The 59 species analyzed in this study include all those gonochoristic fishes for which TSD has been explicitly or implicitly assumed as reported in published reviews on the subject field [12]–[16], as well as in subsequently publications in the chief literature (Table S1). The species are representative of freshwater, estuarine and marine ecosystems. The only hermaphroditic species where TSD has been claimed, the self-fertilizing cyprinodont Kryptolebias (Rivulus) marmoratus, was non included in our report. In this species, there are no females; substantially all individuals develop equally hermaphrodites. Exposure to low temperature during early development increases the proportion of gonochoristic males from ∼3 to 72% [twenty]. Similarly, the Southern brook lamprey, Ichthyomyzon gagei, and the eels, including the American eel, Anguilla rostrata, were not included because the circumstantial bear witness available so far points to growth-dependent sex differentiation [21] rather than to TSD in these species [22], [23].

Information collection

For each species analyzed, field data, including the range of natural temperature in which the species can live (RNT), the range of temperature during development in the wild (RTD) as well as the lethal temperature (LT), when bachelor, were obtained from advert hoc reviews, e.k., [24], Fishbase [25], or specific sources, equally indicated in Table S1. Experimental (generally laboratory) data were also compiled from the principal literature, every bit indicated in Table S1.

Diagnosis of temperature-dependent sex determination (TSD) as opposed to genotypic sex determination plus temperature effects (GSD+TE)

To decide the bodily prevalence of TSD in fish and to replenish robust patterns of sex activity ratio response to temperature, nosotros have used a comparative analysis consisting of the application of two independent criteria to identify the presence of TSD (Fig. 2). The showtime is that of Valenzuela et al. [2], which: (i) stresses that the presence of chromosomal systems of sex decision such as XX/XY or WZ/ZZ, that imply consequent genetic differences between sexes, constitutes a very stiff evidence of the presence of GSD, and thus information technology is extremely unlikely that species with these chromosomal systems have TSD. The testify for sex activity chromosomes may accept been obtained with direct (karyotyping, banding) or indirect methods (e.k., progeny analysis of sexual practice-linked traits, mating experiments or crosses with sex-reversed fish); (ii) considers induced sex ratio shifts that occur simply at extreme (but non defined), ecologically irrelevant temperatures, not proof of TSD. The second criteria, which complements the former, is that of Conover [16], which establishes that in lodge for a species to have TSD, sexual practice ratio shifts in response to temperature fluctuations must occur within a sure range, defined as the range of natural temperature (RNT) in which the species lives. However, since the thermosensitive catamenia in the vast bulk of fish examined so far is usually located during early on development, and particularly during the larval stages [12]–[16], a modification of the benchmark in Conover [16] was used for last assignment of TSD to a given species. Therefore, simply those species for which sex activity ratio shifts occurred not within the RNT but instead within the RTD -the range of temperatures during the period of development that normally includes the thermosensitive period- were considered candidates for having TSD. Particularly in seasonally breeding species of temperate latitudes, RTD is independent within RNT but the opposite is not truthful (Tabular array S1). Thus, response within the RNT is not enough show for TSD. Using the RTD instead of the RNT has the additional advantage of incorporating additional criteria of Valenzuela et al. [2] other than the absence of sex chromosomes, since it facilitates excluding cases of sex reversals induced at extreme temperatures, another possible source of confusion. When a species has a sex chromosomal organisation and/or sexual activity ratio response to temperature occurring at extreme temperatures (sometimes close to the LT), and definitively exterior the RTD (e.grand., Fig. 3B), and hence ecologically irrelevant, then TSD is substantially very unlikely. These instances are more appropriately referred to equally cases of naturally- or experimentally-induced alterations of genotypic sex determination or genotypic sex determination plus temperature effects (GSD+TE) [2], [sixteen] rather than TSD. Thus, for any given species to have TSD, it should fulfill both of the following two conditions: 1) non having sexual activity chromosomes, and 2) accept sex ratio response to temperature within the RTD (Fig. 2). The possible error in proceeding in this mode is negligible and smaller than doing the opposite, i.e., classifying a species as having TSD that has sex chromosomes, which in well-nigh cases is potent evidence of GSD, and/or that exhibits sex ratio shifts at artificially loftier or low temperatures, which is ecologically irrelevant.

Set of criteria used to determine the presence of temperature-dependent sex activity determination (TSD) as opposed to genotypic sex activity determination (GSD), and to distinguish TSD from thermal furnishings on GSD (GSD+TE).

This algorithm is based on the criteria of Valenzuela et al. (2003), and incorporates a modification of the criteria of Conover (2004). See text in the Materials and Methods department for a complete explanation. *Indicates that the prove for a sex chromosomal system may come from direct (karyotyping, banding) or indirect methods (due east.g., progeny assay of sex-linked traits, mating experiments or crosses with sex activity-reversed fish). **Indicates that the sex activity ratio shift must occur within the range of developmental temperatures during development that includes the thermosensitive period (RTD) regardless of whether there is response within the range of natural temperatures where the species lives.

Patterns of sex ratio response to temperature in fish.

A, Examples of authentic cases of TSD following pattern 1, more than males with increasing temperatures. Sex ratio shifts occur inside the range of temperature (shaded areas) normally experienced by fish in the wild. B, Examples of false cases of TSD. Sexual activity ratio shifts only occur at farthermost temperatures, and thus represent thermal furnishings on GSD (a, b). Formerly proposed pattern ii (c), fewer males at high temperature, is non supported by re-analysis of data (see also Supplementary Tabular array 1). C, Formerly proposed pattern 3, more males at farthermost temperatures, tin exist explained from the combination of ii effects unrelated to TSD: tedious growing fish at low temperature differentiating every bit males (a), and the inhibition of aromatase at high temperature causing sex-reversal of genetic females (b). When combined, the two effects result in the observed pattern (c).

Statistical analysis

Sex ratio deviations from ane∶1 in Ictalurus punctatus were checked past applying the Chi-square test [26] to data provided in the original source [27], equally depicted in Table S1.

Sexual practice ratio data originally obtained from monosex (all-female) populations exposed to different temperatures were transformed to make them comparable with data obtained with mixed-sex populations of the same species past applying the following formula: Percent males in a 1∶1 (male person∶female) population = 50+(percent males in the all-female population/2). Thus, for example, an all-female population that at 20°C the percentage of males was 0% and at 28°C was 66% (indicating that two thirds of the females were masculinized) would be equivalent to an 1∶1 population that at xx°C the percent of males was 50% and at 28°C was fifty+(66/2) = 83%. Notice that the possibility of producing all-female stocks is indicative that the species in question has a chromosomal system of sex conclusion, usually of the Twenty/XY type, thus suggesting the presence of GSD rather than of TSD, equally is demonstrated.

The presence of a meaning sex ratio response to temperature inside the RTD and the verification of the presence of TSD in species diagnosed equally having such mechanism of sexual activity determination later applying the criteria explained above was carried out as follows: First, we tested if there was a statistically significant human relationship between sex activity ratio produced and temperature by using the Spearman rank correlation coefficient method. If then, then we compared the slope with the F-test [26] to check whether it was different from zero.

In a few instances, more than than i intermediate temperature has been tested. In these cases, for economy of infinite in the Tabular array S1 merely the average sex ratio value, representative for all the intermediate temperatures, is shown. However, for the regressions, all the available intermediate temperatures were used from the original sources. Besides, each one of the 33 species of the genus Apistogramma studied by Römer and Beisenherz [28] was checked individually and the presence of TSD also confirmed statistically on a ane-by-1 ground, but for simplicity an boilerplate upshot representative of all of them is presented.

In all cases, sex ratio data expressed every bit percentages (i.due east., 100·p, where p is the proportion of males) were arcsin transformed (arcsin of the square root of p) prior to statistical analysis [26]. Statistical analyses and graphs were carried out with the aid of StatGraphics v. v.1 and Graphpad Prism Software 5.iv.0.

Results

Our results show that of the 53–55 species (depending on the authors) previously assigned to design 1, the 33 cichlid species of the genus Apistogramma indeed exhibit blueprint i (Fig. 3A a; Table one) fulfilling the criteria for the assignment of TSD. Nonetheless, merely seven other species of the remaining xx–22 adhere to blueprint ane and accept TSD (Fig. 3A b,c). In all but one of the species with TSD the all-time fit to the experimental information on sex ratio response to temperature was obtained with a linear regression (Y = a+bX). In Menidia menidia, however, the best fit was obtained with a reciprocal-X model (Y = a+b/10) (Fig. 4). Included amidst the species that did not pass the criteria to exist diagnosed as true cases of TSD are some established research models such as the zebrafish (Danio rerio) and the medaka (Oryzias latipes) (Fig. 3B a,b).

Patterns of sex ratio response to temperature in species of fish with TSD.

In all cases, higher temperatures imply a higher number of males produced. Key: 1, Mendia menidia; 2, Odontesthes bonariensis; 3, Hoplosternum littorale; four, Poeciliopsis lucida; v, average of the 33 Apistogramma species; six, Limia melanogaster; 7, Menidia peninsulae; 8, Odontesthes argentinensis.

Regarding blueprint 2, analysis of the original data [27] of channel catfish (Ictalurus punctatus) (Table S1) in fact showed no differences with respect to the 1∶1 sex ratio (Chi-foursquare test = 1.42, P = 0.233) (Fig. 3B c). As well, boosted experiments in sockeye salmon (Oncorhynchus nerka) reported in Azuma et al. [29] (Fig. 3B c) evidenced the presence of pattern one instead of pattern ii, as it had been previously suggested [30]. Nevertheless, both the channel catfish and the sockeye salmon have sex chromosomes and tested temperatures fall outside the natural range (Table 1). Therefore, these are cases of GSD+TE, not of TSD.

Regarding blueprint 3, the ii flatfishes previously assigned to this blueprint (Fig. 3C), the olive flounder (Paralichthys olivaceus) [31] and the Southern flounder (P. lethostigma) [32], each failed 1 of the TSD-determining criteria (Table i).

Based on the relationship between temperature and sexual activity ratio produced as shown in Table 1, we calculated that fish species with TSD exhibit an average (mean±Due south.E.M.) pivotal temperature (PT, temperature that produces balanced sexual activity ratios) of 23.iii±1.5°C (Tabular array two). Then, in the scenario of global warming, nosotros took two temperature increases: 1.5 and 4°C, representative of a very likely increase in temperature of water bodies in the upcoming decades and of the maximum predicted increment by the end of this century [33], respectively. With an increment of just 1.five°C, the boilerplate number of males in the species with TSD would increase to 61.7±ii.one%, and with an increase of four°C, the average number of males would increase to 78.0±4.i%, i.e., the sex ratios (male∶female) would shift from 1∶one to ∼ii∶1 and to ∼iii∶one, respectively (Table ii).

Tabular array ii

Pivotal temperature in fish species with TSD and predicted sex ratio shifts with temperature increases.

Species	Pivotal temp. (°C)	Percent of sexes (♂∶♀) at pivotal temp.+one.5°C	Percentage of sexes (♂∶♀) at pivotal temp.+4°C
Apistogramma spp *	25.3	62 ∶ 38	81 ∶ xix
Hoplosternum littorale	18.8	56 ∶ 44	65 ∶ 35
Limia melanogaster	25.8	57 ∶ 43	68 ∶ 32
Menidia menidia	xiv.5	61 ∶ 39	75 ∶ 25
Menidia peninsulae	26.vi	57 ∶ 43	69 ∶ 31
Odontesthes argentinensis	25.vii	60 ∶ 40	76 ∶ 24
Odontesthes bonariensis	24.2	73 ∶ 27	98 ∶ 2
Poeciliopsis lucida	25.vi	68 ∶ 32	92 ∶ 8
Pivotal temp. (hateful±Southward.E.1000.)	23.3±1.five	-	-
Percent males (hateful±S.Due east.M.)	-	61.7±two.1	78.0±4.1

Discussion

Prevalence of TSD in fish and response patterns

In reptiles, where TSD was first discovered in vertebrates, this mechanism of sex activity determination is now well established (run into the book by Valenzuela and Lance [34], for reviews). In dissimilarity, in fish, the absolute number of studies is more limited and, significantly, only few of them, concerning the Atlantic silversides, take been carried past samplings in the wild [16], while most take been carried out under controlled laboratory atmospheric condition. This may probably reverberate the difficulty of sampling fish at different developmental stages in the wild and, especially, correlating ecology variables during critical thermosensitive periods with resulting sex ratios when adults. However, despite these limitations, this situation did not forbid that TSD was until now considered a widespread machinery of sexual practice decision in fish. Further, based on sex activity ratio response to temperature, fish species where TSD had been claimed had been grouped into iii response patterns.

The assay of sex ratio response to temperature, considering the telescopic of such response also every bit the presence or not of sex chromosomes, carried out in the nowadays study indicated that many species where TSD had been claimed before are in fact GSD species affected by temperature, i.e., cases of GSD+TE. In GSD+TE species, temperature rather than being the external environmental factor controlling sex activity determination is capable of affecting the process of gonadal sex differentiation nether some circumstances. This distinction is not trivial nor semantic since, co-ordinate to the canonical definition [1], in TSD species the first ontogenetic divergence between sexes is an environmental one (temperature), whereas in GSD+TE species sexual practice determination remains under genotypic control.

Our results support the presence of pattern 1 of sex ratio response to temperature (more males with increasing temperature) simply the number of species with TSD is much lower than previously considered and concern mainly species of the families Cichlidae followed past species of the family Atherinopsidae. In addition, nosotros have demonstrated that pattern 2 of sex ratio response to temperature does not be in fish.

Regarding blueprint 3, we propose that this pattern is the result of 2 contained effects unrelated to TSD (Fig. 3C). First, since exposure to low temperatures decreases growth rates in poikylothermic animals, the increment in males at low temperatures is likely the result of male development according to the threshold model for growth-dependent sex differentiation [21]. Briefly, applied here this model states that when a critical time is reached during development, a sexually undifferentiated gonad will develop as an ovary or every bit a testis depending on whether information technology has attained a certain size above or below a threshold, respectively (Fig. 3C a). In fact, a reduction in the number of females was observed among the lower growing fish in the olive flounder, one of the species previously assigned to design three [35]. Although initial exposure to low temperatures in some cases favors female person sex activity differentiation (equally in pattern 1), it is at present known that if such exposure is prolonged, thus delaying growth, so male person sex differentiation occurs [36]. The preponderance of males at depression temperatures too coincides with the left half of pattern 2. Therefore, this pattern sometimes has been also erroneously assigned to species such equally the sea bass (Dicentrarchus labrax) (Table 1), where growth-dependent sex activity differentiation occurs [36]. The other effect, the increase in males at high temperatures in species previously assigned to pattern three, is probable the result of sex-reversal of females every bit a issue of the inhibition of aromatase (Fig. 3C b), the enzyme that produces estrogens essential for female sexual practice differentiation in fish [37]. When combined, the two furnishings produce pattern three (Fig. 3C c). In improver, the observed sex ratio response to temperature, especially in the Southern flounder, partly occurs exterior the RTD, thus not being representative of true TSD. The inhibition of aromatase at high temperatures –and the consequent increase in the number of males- has also been reported in some species without TSD [xv], [38], too explaining why they were assigned to blueprint ane, and, interestingly, as well seen in many species of reptiles [34], [39]. Thus, we discover that only pattern 1 of sex activity ratio response to temperature is present in fish with TSD (Effigy 4), since analysis of the available data does non support the existence of patterns 2 and iii, as accepted until now. This contrasts with the accepted existence of iii response patterns in reptiles [34], although perhaps they should be revisited, every bit done in this report with fish. Further, it has been recognized that the prevalent design in reptiles with TSD is design Ib [xl], which is the equivalent of pattern 1, found to be the only one actually nowadays in fish.

The results of the nowadays written report have implications for our agreement of the evolution of vertebrate sex determining mechanisms. They nevertheless concur with the view that TSD has evolved independently many times [1], [ii], [40], but we find TSD to be present in only iv orders, which include merely 3 of the seven used by Mank et al. [10] to discuss the evolution of sexual activity determining mechanisms specifically in fish. Thus, there is no close relationship amid the families where TSD is present (Fig. five), and many species inside the same families are well known for having GSD, suggesting that TSD is clearly the exception in fish sex determination. The phylogenetic distribution suggests that, when it occurs, TSD in fish is a derived rather than an ancestral machinery. However, at that place are at least 27,977 known species of teleosts [41] and although absolutely the available data on sex determination are a good representation of the biodiversity, information technology has to be borne in mind that the number of species examined is still a minority so far. Thus, the picture shown here may change i twenty-four hours as new species are examined in regards to their sex determination mechanisms.

Distribution of temperature-dependent sex activity conclusion (TSD) in fish.

Orders, families and species with TSD are marked in colour. Teleost phylogeny based on Nelson [41].

What is the reliability of the original information used to assign TSD in the different species that survived our assay? In the species of the F. Atherinopsidae (silversides) the testify seems robust [11], [13], [16], [xviii], [nineteen], but it should be remembered that the species of the genus Odontesthes data has been obtained from laboratory experiments. In the genus Apistogramma (South American Cichlids), TSD was demonstrated in many species and thus besides seems well established, although the prove gathered then far originates from a single study [28]. The same state of affairs applies for the atipa, Hoplosternum littorale, an Amazonian freshwater fish, where several batches of eggs were used and tested temperatures corresponded to the natural fluctuation; yet, data originates from a single study [42]. In contrast, information concerning Poeciliopsis lucida, a freshwater fish from Mexico, not only comes from a single study [43] simply also the two strains used were highly inbred, one responding to temperature and the other not. The sometime passed the criteria for existence classified as TSD but whether similar results would be obtained with other strains remains to exist determined. Further, this is a viviparous species, and viviparity seems incompatible with the requirements to develop TSD [two]. Thus, further research would be necessary to establish whether P. lucida has populations with GSD and others with TSD or whether information technology is a GSD+TE species.

The criteria used hither allow the identification of the presence of TSD in a given species. However, this does not exclude the possibility that these species may also take populations with GSD. Therefore, populations with GSD and TSD may co-exist in a unmarried species [16]. Here it is interesting to notice that fifty-fifty in these cases, the pattern of sex ratio response to temperature is invariably pattern 1. On the other hand, it should exist noted that the identification of sex activity chromosomes, specially if they are homomorphic, tin can depend on the sensitivity of the method used to search for them. Thus, the number of species with TSD may be further reduced in the futurity as new technical developments, such as new fluorescent molecular probes, increase our ability to find sex chromosomes.

The tilapias (genus Oreochromis) deserve special attention, not but because their importance for aquaculture just also because some of them constitute established inquiry models where many studies on the effects of temperature in fish sex differentiation have been carried out [12]–[15]. Tilapias did not pass our criteria to be considered TSD species because there are genetic differences between sexes that can be discerned with straight and indirect methods. In fact, currently the genetic sexual activity determinism of tilapias is condign well understood [44]. Further, recent studies accept shown that some tilapia populations adapted to extreme conditions tin can tolerate temperatures close to 40°C and take rightly pointed out that high temperature influences the normal grade of sex differentiation with the resulting masculinization of genetic females [45]. Thus, in accordance with the definitions used here and elsewhere [2], tilapias, then, are a prime example of GSD+TE species, but non of TSD species. To avoid confusion, so, if for a given species there is no compelling evidence of the presence of TSD is better to use the term "temperature furnishings on sex ratios" or "temperature furnishings on sex activity differentiation", but non "temperature-dependent sexual practice determination".

TSD in fish and climate change

How species with TSD will reply to current rapid climate change is a timely question [3], [nine], [40]. Some data is available for sea turtles with TSD [8], [nine] but is non-existent for fish. Based on the information gathered in the present report some predictions can be made, although it should be taken into business relationship that they are based on a simple linear correlation between temperature and resulting sex ratio. However, in the absence of field data, they are the best educated guess one tin make based on the information available so far.

The species identified as having TSD in this report found a heterogeneous group since they include both freshwater and marine species living besides both in low and high latitudes. Some of them are typically eurithermal while others are stenothermal and, farther, they showroom different reproductive strategies.

Similarly, global warming is not a heterogeneous procedure, since it affects different parts of the Earth differently. Globally, yet, hateful temperatures of water bodies are projected to increase by upward to ∼4°C by the end of this century according to plausible global alter scenarios [33]. Even pocket-size changes of 1–two°C may significantly skew the sex activity ratio, as already shown in field studies with turtles [three] and sea turtles [ix]. In fish, observations made with 1000. menidia eggs collected from the wild have shown that differences of 2°C during the thermosensitive period can result in sex ratio shifts from l% to 69% males [xix].

Thus, the number of females in species with TSD, some of which are of economic or recreational importance, could subtract. One such species is the Argentinean silverside (O. bonariensis), where recent studies propose thermal effects on gonadal development already occurring in natural populations [46]. The species with the to the lowest degree pronounced slopes in the relationship betwixt temperature and the sexual activity ratio produced would be less affected or non affected at all. In O. bonariensis, an increase of just 1.v°C could shift the pct males from an average of l% to ∼73%, that is, from 1∶1 to ∼iii∶one. Since the reproductive potential of many fish communities is determined by the number of females available for egg production [47], highly male person-biased sexual practice ratios would likely affect population structure and the viability of sensitive stocks.

Potential temperature effects on sex ratios could exist difficult to quantify if they are mitigated by other global warming-induced furnishings, including species distribution shifts [4]. In addition, skewed sex ratios may favor frequency-dependent selection of the less abundant sex, the development of TSD towards its disappearance or adjustments in the pivotal temperature [48]. In contrast to by, naturally occurring fluctuations of global temperature, the electric current climate change result with anthropogenic influences is characterized by its fast pace [33]. Thus, it has been suggested that sensitive species, including species with TSD, could non accommodate fast plenty to the rapid change in temperatures brought by the new thermal situation [iii].

It should exist noted that the impact of temperature on sex ratios could besides touch on species with identifiable sex activity chromosomes (by causing sexual practice reversal) provided that those effects occur at temperatures within the natural range, or the new shifted range. Notwithstanding, at this point there is insufficient information to determine if, past virtue of their possible college sensitivity to temperature, species with TSD are amend indicators of the impacts of climate change on sex ratios than GSD+TE species.

Conclusions

In this study, we performed an assay of field and laboratory data related to fish species for which TSD was assumed. Past applying a series of criteria accepted to define the actual presence of TSD, we can reasonably affirm that, excluding the species of the genus Apistogramma, in approximately 75% (19 out of 26) of the species considered to have TSD so far, observed sex activity ratio shifts at farthermost temperatures are most probable the outcome of thermal effects on GSD rather than proof of the existence of TSD. Thus, in that location may be species in which TSD has not yet been discovered but, contrary to the prevailing view, TSD in fish is not as widespread as currently thought, and, importantly, simply ane full general pattern of sex activity ratio response to temperature exists. However, species which do possess TSD, or species with GSD+TE, may compromise their viability by diminishing the number of females in response to even small increases in water temperatures.

Supporting Information

Tabular array S1

Temperature-Dependent Sex Decision in Fish. Prevalence, Beingness of a Single Sex Ratio Response Pattern, and Possible Effects of Climate Change.

(0.35 MB DOC)

Acknowledgments

We would like to thank the following persons: M. Blázquez, J. Cerdà, North. Mrosovsky, S. Sarre, M. Schartl and J. Viñas for helpful comments; F. Mayou for providing advice on statistical analyses; and J.I. Fernandino for providing information on Odontesthes sp.

Footnotes

Competing Interests: The authors take alleged that no competing interests exist.

Funding: Piece of work supported past a Spanish Ministry of Education and Science grant ("Sexratio") to F.P. N.O.A. was supported by a scholarship from the aquaculture network (XRAq) from the Regime of Catalonia.

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