Skip to main content
NCBI home page
Ecology and Evolution logoLink to Ecology and Evolution
. 2017 Jan 13;7(3):905–917. doi: 10.1002/ece3.2572

The interplay between natural and sexual selection in the evolution of sexual size dimorphism in Sceloporus lizards (Squamata: Phrynosomatidae)

Víctor H Jiménez‐Arcos 1, Salomón Sanabria‐Urbán 1, Raúl Cueva del Castillo 1,✉
PMCID: PMC5288261  PMID: 28168027

Abstract

Sexual size dimorphism (SSD) evolves because body size is usually related to reproductive success through different pathways in females and males. Female body size is strongly correlated with fecundity, while in males, body size is correlated with mating success. In many lizard species, males are larger than females, whereas in others, females are the larger sex, suggesting that selection on fecundity has been stronger than sexual selection on males. As placental development or egg retention requires more space within the abdominal cavity, it has been suggested that females of viviparous lizards have larger abdomens or body size than their oviparous relatives. Thus, it would be expected that females of viviparous species attain larger sizes than their oviparous relatives, generating more biased patterns of SSD. We test these predictions using lizards of the genus Sceloporus. After controlling for phylogenetic effects, our results confirm a strong relationship between female body size and fecundity, suggesting that selection for higher fecundity has had a main role in the evolution of female body size. However, oviparous and viviparous females exhibit similar sizes and allometric relationships. Even though there is a strong effect of body size on female fecundity, once phylogenetic effects are considered, we find that the slope of male on female body size is significantly larger than one, providing evidence of greater evolutionary divergence of male body size. These results suggest that the relative impact of sexual selection acting on males has been stronger than fecundity selection acting on females within Sceloporus lizards.

Keywords: dimorphism, fecundity, Lizards, natural selection, Rensch's rule, Sceloporus, sexual selection

1. Introduction

In animal species that reproduce sexually, adult males and females often differ in body size. This difference is termed sexual size dimorphism (SSD) and generally evolves because body size is commonly related to reproductive success through different pathways in females and males (Blanckenhorn, 2005; Fairbairn, Blanckenhorn, & Székely, 2007). In females, body size is strongly correlated with fecundity, whereas in males, body size is correlated with mating success. As result of these differences, the body size that conveys maximal fitness often differs between the sexes (Fairbairn et al., 2007). The impact of sexual selection on SSD has been well established in many studies of individual species as well as in many phylogenetically controlled comparisons among species (Andersson, 1994; Fairbairn, 1997; Fairbairn et al., 2007). In addition, fecundity selection favors large female body size in species where females mature large numbers of eggs or live young within their abdomens, as in most fish, insects, and spiders (Blanckenhorn, 2005; Fairbairn, 1997; Fairbairn et al., 2007; Ruckstuhl & Neuhaus, 2005). SSD also can arise through ecological niche divergence, such as sex‐specific foraging/dispersal strategies or adaptations to reduce intersexual trophic competition (reviews in Blanckenhorn, 2005; Fairbairn, 1997; Fairbairn et al., 2007; Hedrick & Temeles, 1989; Reiss, 1989; Ruckstuhl & Neuhaus, 2005; Shine, 1989). However, it is unlikely that niche divergence between males and females is truly independent of sexual divergence in reproductive roles (Butler & Losos, 2002; Butler, Schoener, & Losos, 2000; Fairbairn et al., 2007).

In many vertebrate and invertebrate taxa, the magnitude of SSD changes systematically with mean body size, either increasing or decreasing as body size increases (Fairbairn et al., 2007; Webb & Freckleton, 2007). The former pattern is common in species where males are larger than females, while the latter occurs commonly in species in which females are the larger sex. Both patterns are explained by greater evolutionary divergence in male size, compared with female size; a pattern known as Rensch's rule (Fairbairn, 1997; Rensch, 1950). This allometric trend is usually attributed to sexual selection acting on male body size (Fairbairn et al., 2007; Stillwell et al., 2010). The converse trend, where female size varies more than male size, is less common, but seems to be the result of strong fecundity selection acting on females (Fairbairn et al., 2007; Foellmer & Moya‐Laraño, 2007; Webb & Freckleton, 2007). Lizards exhibit a broad range of SSD. However, in the majority of species, males are larger than females (Cox, Butler, & John‐Alder, 2007; Cox, Skelly, & John‐Alder, 2003), mainly because body size often determines success in agonistic encounters, and it is correlated with dominance and territoriality (Carpenter, 1995; McMann, 1993; Molina‐Borja, Padron‐Fumero, & Alfonso‐Martin, 1998; Perry et al., 2004). Nonetheless, in some species, females are larger than males, suggesting that fecundity selection may have favored the evolution of large female body size because it may allow females to (1) accommodate more offspring (Cox et al., 2003; Stuart‐Fox, 2009; Zamudio, 1998) and (2) increase the capacity for storing energy to be invested in reproduction (Calder, 1984; Pincheira‐Donoso & Tregenza, 2011).

Lizards species can be oviparous or viviparous (Blanckenhorn, 2000; Méndez–de la Cruz, Villagrán‐Santa Cruz, & Andrews, 1998). In some viviparous species, the embryos develop in a placenta with little or no shell forming, whereas in other species, the female retains the eggs within the uterus until development is complete. In any case, because placental gestation or extended egg retention requires more space within the abdominal cavity associated with an increased gestation period (Pincheira‐Donoso & Tregenza, 2011; Qualls & Shine, 1995), it has been suggested that the females of viviparous lizards possess larger body size or greater abdomens than their oviparous relatives (Braña, 1996; Scharf & Meiri, 2013; Yan‐Yan et al., 2012).

The lizard genus Sceloporus serves as an excellent example of SSD in lizards. This is a widely distributed genus (from southwestern Canada to northern Panama), which can be found in several environments and along broad altitudinal ranges (0 to >4,000 m; Sites et al., 1992; Smith, 1939). There are both oviparous and viviparous species in the genus (Méndez–de la Cruz, Villagrán‐Santa Cruz & Andrews, 1998). In the majority of species, males are the larger sex and exhibit a conspicuous coloration formed by belly and gular patches. However, these characteristics are also present in the females of some species within the group (Calisi & Hews, 2007; Carpenter, 1978; Fitch, 1978; Jiménez‐Cruz et al., 2005; Köhler & Heimes, 2002; Ramírez‐Bautista & Pavón, 2009; Ramírez‐Bautista et al., 2008; Ramírez‐Bautista, Stephenson, Lozano, et al., 2012; Weiss, 2006). In addition, conspicuous coloration is also present on the dorsum, including the head, tail, and limbs (e.g., Sceloporus minor, S. aureolus, S. horridus: Köhler & Heimes, 2002; Stephenson & Ramírez‐Bautista, 2012). The sexual coloration in males, principally the belly and gular patches, is related to species recognition, territory defense, agonistic interactions, and courtship (Carpenter, 1978; Martins, 1994; Sites et al., 1992; Wiens, Reeder, & Nieto Montes de Oca, 1999), which suggests that sexual selection has generated much of the divergence among males and females in Sceloporus lizards. However, in other species, females are larger than males (Fitch, 1978), suggesting that in these species, selection on female fecundity has been stronger than sexual selection on males.

In this study, we explore the relationship between female body size, fecundity and reproductive modes, and the potential impact of these relationships on body size divergence between females and males of Sceloporus lizards. In addition, we tested Rensch's rule in order to evaluate the relative impact of sexual selection on the evolution of SSD, and we performed an ancestral character reconstruction to infer the evolutionary trends of SSD in these lizards. We expected differences in body size between oviparous and viviparous females and that these differences affect the body size relationships between the sexes. Nonetheless, if sexual selection has been the main force driving the evolution of SSD in Sceloporus, we predict that the regression of male size on female size will have a slope steeper than 1, following the Rensch's rule.

2. Methods

2.1. Data collection

Our study comprised data collected for 56 Sceloporus species, four Urosaurus species and Petrosaurus thalassinus for a total of 61 evolutionary units (Urosaurus and P. thalassinus were used as outgroup taxa). The Sceloporus species sampled included all major species groups of the genus (Leaché, 2010; Wiens et al., 2010); 41 species were oviparous and 20 were viviparous (Table 1). We performed a literature search for data on snout‐vent length (SVL; a standard measure used as a proxy for lizard size; Cox et al., 2003; Losos, 1990) for both females and males and clutch/litter sizes (number of eggs or embryos) for the species studied. We collected information from the literature by executing searches on Google Scholar using the terms “snout‐vent length,” “clutch size,” “litter size,” “number of eggs/embryos,” “sexual size dimorphism,” or “reproductive cycle” for a list of species of the genus Sceloporus, reported by Wiens, Kozak, and Silva (2013). Google Scholar was used as the search engine instead of other engines because it cataloged full‐text versions of published papers. Moreover, terms that were included in our search like “clutch size,” “litter size,” and “snout‐vent length” were not the principal focus of the papers, and the phrases were usually referred to only briefly. Thus, we were less likely to locate the pertinent information using literature databases that contain only keywords, titles, and abstracts (see Dornhaus, Powell, & Bengston, 2012). We excluded data in which the number of vitellogenics follicles were reported as part of clutch size, because the follicular atresia may occur in any stage of the ovogenesis, including previtellogenic and vitellogenic follicles, and thus does not represent an accurate estimation of clutch/litter size (Méndez‐de la Cruz et al., 2013). For species with data on more than one clutch per reproductive season, we used the average of all clutches reported in the literature.

Table 1.

Mean snout‐vent length (SVL), clutch/litter size, and reproductive mode (O = oviparous and V = viviparous) for 56 Sceloporus species and five outgroup taxa

Species SVL females (mm) SVL males (mm) Clutch size Reproductive mode References
Petrosaurus thalassinus 99.15 (71–110) (44) 107.23 (80–152) (44) 8.6 (4–18) (10) O Goldberg and Beaman (2004)
Sceloporus adleri 63.11 (54–78.8) (23) 65.28 (59–72) (14) 6.57 (2–11) (14) V Fitch (1978), Santos‐Bibiano (unpublished data)
S. aeneus 51.88 (43.4–59.1) (194) 52.98 (43.4–62.8) (138) 7.3 (7–12) (32) O Jiménez‐Arcos (2013)
S. angustus 62.8 (61–66) (5) 78.2 (65–86) (6) 5.5 (4–7) (5) O Goldberg (2014)
S. arenicolus 53.8 (49–62.2) (339) 54.5 (49–64.9) (507) 5 (4–6) (?) O Fitzgerald et al. (2011)
S. bicanthalis 51.84 (42.4–58) (85) 43.6 (42–53.2) (42) 7.18 (3–9) (68) V Rodríguez‐Romero et al. (2010), This studya
S. chrysostictus 51.3 (82) 53.95 (82) 2.4 (1–4) (16) O Fitch (1985), Köhler and Heimes (2002)
S. clarkii 88.08 (72–120) (57) 103 (91–138) (56) 10.85 (1–24) (39) O Fitch (1978, 1985), Parker and Pianka (1973)
S. consobrinus 68.4 (54–77) (58) 60.5 (50–68) (44) 9.9 (39) O Vinegar (1975a)
S. couchii 50 (36) 58 (32) 4 (?) O García de la Peña et al. (2004), Lemos‐Espinal and Smith (2007)
S. cozumelae 45.48 (41–57) (33) 50.72 (43–60) (57) 1.8 (12) O Fitch (1978)
S. cryptus 67.06 (58.5–76.6) (8) 61.6 (58.9–68.5) (6) 9 (6–12) (4) V This studyb
S. cyanogenys 63 (15) 66 (15) 16.45 (6–18) (36) V Fitch (1985), García‐de la Peña, Castañeda, and Lazcano (2005)
S. dugesii 61.5 (50–78) (91) 65.9 (50–98) (73) 4.4 (1–10) (27) V Ramírez‐Bautista and Dávila‐Ulloa (2009)
S. edwardtaylori 107 (?) 107 ? 8.5 (8–9) (2) O Köhler and Heimes (2002)
S. for. formosus 67.46 (50–83.3) (113) 67.98 (50–87.4) (99) 8.63 (6–18) (16) V Ramírez‐Bautista and Pavón (2009), This studyb
S. for. scitulus 66.49 (62.5–84.9) (82) 70.88 (63.3–87.3) (73) 6.04 (2–12) (27) V Ramírez‐Pinilla et al. (2009), This studya
S. gadoviae 54.95 (45.7–57.2) (6) 64.9 (69.6–73.5) (6) 3.6 (1–5) (20) O Lemos‐Espinal, Smith, and Ballinger (1999), This studya
S. graciosus 57.59 (48–69) (197) 55.18 (48–63) (182) 4.55 (1–10) (381) O Burkholder and Tanner (1974), Fitch (1978, 1985), Tinkle (1973)
S. grammicus 56.05 (42.1–72.5) (278) 60.06 (45–79.9) (412) 5.35 (2–12) (167) V Ramírez‐Bautista, Stephenson, Hernández‐Íbarra, et al. (2012), Ramírez‐Bautista, Stephenson, Lozano, et al. (2012), This studya
S. grandaevus 58.5 (58–59) (2) 72.1 (67–78) (5) 6.5 (6–7) (2) O Goldberg (2014)
S. horridus 82.17 (60–100) (46) 85.49 (52–118) (82) 14 (7–18) (16) O Valdéz‐González and Ramírez‐Bautista (2002), This studya
S. hunsakeri 64.13 (19) 73.96 (20) 7.5 (5–10) (2) O Galina Tessaro et al. (2015)
S. jalapae 46 (42–50) (24) 49.3 (45–62) (17) 5.6 (4–8) (10) O Ramirez‐Bautista et al. (2005)
S. jarrovii 66.21 (60–86) (787) 69.67 (46–98) (668) 7.35 (2–16) (405) V Ballinger (1973), Gadsden and Estrada‐Rodríguez (2007)
S. licki 63.83 (13) 71.46 (24) 6 (?) O Galina Tessaro et al. (2015)
S. macdougalli 83.84 (72.5–95.4) (29) 88.82 (81.8–92.5) (7) 3.88 (2–5) (9) V Martínez Bernal (2004)
S. magister 93.64 (80–120) (54) 111.45 (80–140) (53) 6.98 (2–12) (43) O Fitch (1978, 1985)
S. malachiticus 75.49 (64–86) (208) 79.12 (67–90) (146) 6 (3–10) (44) V Fitch (1978, 1985)
S. megalepidurus 44.99 (37–48) (36) 47.28 (39–55) (76) 2.04 (1–4) (25) V Fitch (1978), Godinez‐Cano (1985)
S. melanorhinus 87.9 (62–98) (30) 84.6 (62–95) (32) 7.7 (5–9) (12) O Ramirez‐Bautista et al. (2006)
S. merriami 48.13 (39–55) (164) 52.24 (42–61) (355) 4.33 (2–7) (127) O Fitch (1978), Grant and Dunham (1990)
S. minor 65.65 (41.6–92.9) (182) 70.32 (53.6–99.4) (169) 6.09 (2–13) (46) V Ramírez‐Bautista et al. (2008, 2014)
S. mucronatus 78.89 (56.5–102) (170) 87.02 (55.2–111.2) (146) 5.8 (2–13) (49) V Ortega‐León et al. (2007), Villagrán‐Santa Cruz et al. (2009), This studya
S. nelsoni 52.14 (48–58) (21) 60.15 (53–65) (26) 6.25 (4–8) (4) O Fitch (1978)
S. occidentalis 74.63 (68–87) (43) 68.35 (61–81) (46) 8.12 (3–14) (243) O Fitch (1978), Herrel, Meyers, and Vanhooydonck (2002)
S. ochoterenae 44.39 (31–67) (110) 48.23 (44–56) (143) 6.77 (3–7) (35) O Bustos‐Zagal et al. (2011), Smith and Lemos‐Espinal (2003)
S. olivaceus 93 (63–107) (107) 82.9 (60–93) (34) 14.3 (8–30) (14) O Blair (1960)
S. omiltemanus 83.08 (39) 98.11 (25) 6.23 (6–8) (13) V Ramírez‐Pinilla et al. (2009)
S. orcutti 92 (85–106) (77) 102 (90–115) (17) 11 (8–15) (4) O Mayhew (1963)
S. parvus 46.85 (44.7–49) (?) 50 (?) 3.8 (>2) O García‐Vázquez, Trujano‐Ortega, and Contreras‐Arquieta (2014), Lemos‐Espinal and Dixon (2013)
S. pictus 47.86 (44–52) (7) 48.88 (47–51) (8) 3.6 (2–6) (5) V Fitch (1978)
S. poinsettii 89.45 (79–116) (55) 96.79 (77–130) (79) 10.5 (4–23) (90) V Fitch (1978, 1985), Gadsden et al. (2005)
S. pyrocephalus 53.41 (47–62) (88) 62.01 (50–75) (84) 5.65 (4–9) (24) O Fitch (1978), Ramírez‐Bautista and Olvera Becerril (2004)
S. spi. caeruleopunctatus 87.22 (77–96) (18) 88.29 (82–99) (17) 12.82 (8–19) (23) O Calderón‐Espinosa, Andrews, and Méndez de la Cruz (2006), Fitch (1978)
Sceloporus spi. spinosus 91.11 (65.7–110.5) (164) 92.66 (60–112) (164) 14.09 (6–22) (38) O Méndez de la Cruz et al. (2013), Ramírez‐Bautista, Stephenson, Hernández‐Íbarra, et al. (2012), Ramírez‐Bautista, Stephenson, Lozano, et al. (2012), Ramírez‐Bautista et al. (2014), Valdéz‐González and Ramírez‐Bautista (2002)
S. scalaris 51.25 (40–60) (203) 45.53 (40–55) (45) 8.28 (4–15) (109) O Carbajal‐Márquez and Quintero‐Díaz (2013), Fitch (1978, 1985), Vitt (1977)
S. siniferus 49.88 (40–61) (139) 52.49 (53–61) (235) 4.94 (2–8) (15) O Fitch (1978), Ramírez‐Bautista et al. (2015)
S. smaragdinus 62.24 (55–77) (17) 67.22 (60–80) (14) 4.2 (3–6) (10) V Fitch (1978)
S. subpictus 66.47 (63.1–69) (41) 63.54 (1) 13 (12–14) (2) V This studyb
S. torquatus 94.03 (65–110) (4) 101.51 (43.2–115.9) (37) 7.78 (3–17) (84) V Feria Ortiz, Salgado Ugarte, and Nieto‐Montes de Oca (2001), Guillette and Méndez‐de la Cruz (1993), This studya
S. tristichus 63.3 (48–67) (57) 55.9 (53–73) (54) 7.2 (29) O Vinegar (1975b)
S. undulatus 61.11 (53–72) (118) 55.78 (45–65) (177) 8.02 (3–15) (376) O Fitch (1978, 1985), Herrel et al. (2002)
S. utiformis 63.41 (51–73) (104) 61.25 (45–84) (122) 6.94 (3–10) (31) O Fitch (1978), Ramírez‐Bautista and Gutiérrez‐Mayén (2003)
S. variabilis 52.65 (44–68) (424) 61.99 (42–74) (457) 3.92 (1–7) (216) O Benabid (1994), Cruz‐Elizalde & Ramírez‐Bautista (2016 and references in table 6), Fitch (1978, 1985)
S. virgatus 63.81 (51–74.2) (54) 50.42 (48–58) (22) 9.44 (4–16) (228) O Abell (1999), Herrel et al. (2002), Vinegar (1975a)
S. woodi 57.24 (64) 51.89 (78) 4.62 (2–8) (231) O Jackson and Telford (1974), Williams (2010)
Urosaurus bicarinatus 45.84 (40–53) (249) 49.66 (38–61) (322) 6.26 (2–11) (50) O Ramírez‐Bautista, Uribe‐Peña, and Guillette (1995), Ramirez‐Bautista and Vitt (1998)
U. graciosus 38.69 (44–66) (60) 62.35 (42–66) (42) 4.05 (2–10) (25) O Fitch (1985), Vitt, Van Loben Sels, and Ohmart (1978)
U. nigricaudus 51.82 (44–60) (121) 62.47 (57.2–65.4) (42) 4.05 (2–6) (25) O Romero‐Schmidt, Ortega‐Rubio, and Acevedo‐Beltran (1999)
U. ornatus 49.98 (45–58) (14) 50.87 (47–60) (34) 7.25 (2–12) (1454) O Fitch (1985), Martin (1973), Van Loben Sels and Vitt (1984)
Open in a new tab

Size and clutch/litter size ranges are shown in parentheses below mean values. Numbers between parentheses refer to sample sizes. The symbol (?) represents a lack of sample size data in the literature.

a

Only SVL data obtained in this study.

b

Both SVL and litter size data obtained in this study.

In addition to this data set, we incorporated unpublished measurements collected by us from the individuals of ten species. Both SVL and litter size data were incorporated for S. cryptus, S. formosus formosus, and S. subpictus (all viviparous species). SVL data from both sexes were collected for S. bicanthalis, S. formosus scitulus, S. gadoviae, S. grammicus, S. horridus, S. mucronatus, and S. torquatus. Litter size was obtained from direct observations of females giving birth in captivity (see Bastiaans et al., 2014 for care details). Digital calipers were used to take SVL measurements to the nearest 0.1 mm (Mitutoyo CD‐15DC; Mitutoyo Corp., Tokyo, Japan). All lizards captured for this study were unharmed and released at their original capture locations following data collection.

The number of eggs or embryos was used as an estimation of fecundity. Prior to further analyses, all measurements were log10‐transformed to improve linear fits. In addition, we estimated a sexual size dimorphism index (SDI) on SVL following the Lovich and Gibbons (1992) criteria. This index expresses SSD as [(length of larger sex/length of smaller sex) − 1]. For convention, the SDI is arbitrarily changed to negative when males are the larger sex and positive when females are the larger sex (Cox et al., 2007).

2.2. Phylogenetic reconstruction

We inferred the phylogenetic relationships between the 56 studied species of Sceloporus using the nucleotide sequences of eight nuclear (BDNF, ECEL, PNN, PRLR, PTPN, R35, RAG1, TRAF6) and five mitochondrial genes (12S, 16S, ND1, ND2, ND4) available on GenBank. We also retrieved the same genetic information from five outgroup taxa which included four Urosaurus species, representing the sister group of Sceloporus (Leaché, 2010; Wiens et al., 2010) and Petrosaurus thalassinus. The number of species sampled for each gene was BDNF = 48, ECEL = 25, PNN = 47, PRLR = 27, PTPN = 26, R35 = 48, TRAF6 = 46, 12S = 57, 16S = 56, ND1 = 54, ND2 = 35, and ND4 = 57. All matrices were similar to previous studies (Leaché, 2010; Wiens et al., 2010). However, we treated the two subspecies of S. formosus (i.e., S. formosus formosus and S. formosus scitulus) as putative species based on previous evidence for distinct lineages (Pérez‐Ramos & Saldaña de La Riva, 2008; Wiens & Reeder, 1997). A similar situation is present in S. spinosus (with S. spinosus spinosus and S. spinosus caeruleopunctatus). Wiens et al. (2010) recognized these taxa as putative species, which was also supported by more recent evidence (Grummer et al., 2015). Our inclusion of these taxa as distinct evolutionary lineages was not an endorsement of their recognition as different species, but we did not want to ignore important previous taxonomic work on these groups (see Pérez‐Ramos & Saldaña de La Riva, 2008; Wiens & Reeder, 1997; Wiens et al., 2013).

We used MUSCLE algorithm (Edgar, 2004) to align each gene data set using the default parameters in the software MEGA (version 7; Kumar, Stecher, & Tamura, 2016). We then used the software MESQUITE (Maddison & Maddison, 2015) to combine the sequences of each gene, and to make the final concatenated matrix for all genes (see below). We provide the GenBank accession numbers of the sequences used in Appendix S1. Our concatenated alignment consisted of genetic information from 61 terminals (56 Sceloporus species, five outgroups taxa) and 11,113 characters. We estimated the best partition scheme and nucleotide substitution models for the data using the greedy algorithm of PARTITIONFINDER (version 1.1.1; Lanfear et al., 2014). We conducted a concatenated Bayesian inference (BI) analysis in MRBAYES (version 3.2.6; Ronquist et al., 2012) by applying the specific substitution model estimated for each partition. The BI analysis consisted of four independent runs, each with 10,000,000 generations and four chains, sampling every 1,000 generations. We used default priors for other parameters in the analysis. We assessed parameter convergence and proper mixing of independent runs using TRACER (version 1.6; Rambaut & Drummond, 2013). All parameter values sampled during the MCMC of the analysis resulted in ESS values greater than 200. We discarded 25% of the samples obtained prior to stability as burn‐in to obtain a final consensus tree (See Appendix S1 for details).

Our analysis only considered the phylogeny that resulted from a concatenated matrix of both mitochondrial and nuclear loci, utilizing a total evidence approach for Sceloporus species and outgroup taxa. Although this approach may be controversial because nuclear and mitochondrial genes may have incongruent histories due to incomplete lineage sorting and exhibit different substitutions rates (see Maddison, 1997), concatenated matrices have improved the resolution of the phylogenetic relationships of phrynosomatid lizards (Wiens et al., 2010). Moreover, our phylogenetic results were largely congruent with a recent phylogenetic study on Sceloporus that involved a wider taxonomic and genetic sampling, as well as different methodological approaches (concatenation and coalescent‐based methods) to infer phylogenetic relationships (Leaché et al., 2016).

2.3. Comparative analyses

We converted the molecular branch lengths from the Bayesian analysis to units of time using a penalized likelihood method (Sanderson, 2002). For branch length conversion, we used the R (version 3.1.3; R Core Team 2015) package “ape” (Paradis, Claude, & Strimmer, 2004) and performed all the comparative analysis on the resulting ultrametric phylogeny. For more details, see Appendix S1.

2.4. Reproductive modes, female body size, fecundity, and SDI

We used the phylogenetic generalized least squares (PGLS) model to test for an association between fecundity, body size, and reproductive mode. The PGLS approach incorporates phylogenetic information into linear models to account for the statistical nonindependence of residuals using a variance–covariance matrix (see Martins & Hansen, 1997) specified by the phylogeny. For all models, the maximum likelihood value of the weighting parameter λ was estimated simultaneously with the models (Gonzalez‐Voyer & Kolm, 2010; Revell, 2010). The λ parameter indicates whether trait evolution is independent of the phylogeny (λ = 0) or evolving according to Brownian motion (λ = 1). Intermediate values of λ suggest a process in which the effect of the given phylogeny is weaker than expected by Brownian motion evolution (Pagel, 1999). The models were fitted as implemented in the R package “caper” (Orme et al., 2012). The first model included fecundity (dependent variable), log10 SVL female (independent variable), and reproductive mode (categorical independent variable) as well as the interaction between SVL and reproductive mode. In order to evaluate the impact of fecundity on SDI, we first saved the residuals of the previous model and then constructed a model with SDI as the dependent variable, reproductive mode as a categorical independent variable, and the fecundity residuals as a covariate. We used the residuals to eliminate potential confounding effects associated with female body size.

2.5. Rensch's rule and ancestral reconstruction of SDI

Rensch's rule predicts that the slope of a regression of male body size on female body size will be steeper than 1. To test this prediction in the studied species, we used the phylogenetic independent contrasts method (PIC method; Felsenstein, 1985), as implemented by the R package “caper” (Orme et al., 2012) to control for the phylogenetic nonindependence of species (Harvey & Pagel, 1991). We examined the studentized residuals for outliers > |±3|, but found none in our data set. Also, in order to verify whether the standardized contrasts are independent from their estimated nodal values (see Felsenstein, 1985), we plotted the standardized contrasts against their estimated nodal values using the “plot” function provided by “caper”. Ultimately, we tested the allometric relationship between independent contrasts of log10 SVL male (dependent variable) and log10 SVL female (independent variable) by fitting major axis regression using the R package “smatr” (Warton et al., 2012). Major axis regression offers an accurate approach to test the null hypothesis of isometry (h0: β = 1), because both variables were measured on the same scale and residual variance is minimized in both x and y dimensions, rather than the y dimension only (Cox et al., 2007; Pincheira‐Donoso & Tregenza, 2011; Warton et al., 2006). Given that the mean value of contrasts is expected to be zero (Sanabria‐Urbán et al., 2015), we forced the major axis regression through the origin. We used the Wald statistic (r w) and confidence intervals (95%) of the slope to test the null hypothesis (see Warton et al., 2006). In addition, in order to explore the evolutionary trends in body size and SDI, we performed an ancestral character reconstruction following Revell (2013). This method estimates the maximum likelihood value for internal nodes and then interpolates the states along the branches of the tree (see Revell, 2013, 2014 for details). For the reconstruction and visualization of ancestral state reconstruction of SDI (see Figure 3), we used the R package “phytools” (Revell, 2012).

Figure 3.

Figure 3

Open in a new tab

Maximum likelihood ancestral reconstruction of SDI for 56 species of Sceloporus and five outgroup taxa performed in R package “phytools” (Revell, 2012). For the analysis, we used the ultrametric phylogeny and the values of SDI estimated for each species. The values in the color ramp represent the range of SDI registered for the study species. Negative values indicate male‐biased SSD (blue to paleyellow) and positive values female‐biased SSD (palepurple to red). Open and filled circles indicate, respectively, oviparous and viviparous lizard species

3. Results

3.1. Reproductive modes, body size, and fecundity

After controlling for phylogenetic nonindependence among of the species studied, the results of the PGLS analysis were highly significant (r 2 = 0.3, F 3,57 = 8.025, p = .0001). We found a strong and significantly positive relationship between body size and fecundity (β = 0.98 ± 0.26, t = 3.801, p = .0003; Figure 1). Nonetheless, there were no differences in fecundity between reproductive modes (β = −0.15 ± 0.85, t = −0.174, p = .86). The interaction between reproductive modes and body size was not significant (β = 0.04 ± 0.47, t = 0.086, p = .93), indicating a similar fecundity response to an increase in the body size of both oviparous and viviparous species. The model showed intermediate λ values (λ = 0.54), indicating a relatively weak phylogenetic effect on the relationships between body size and fecundity.

Figure 1.

Figure 1

Open in a new tab

The relationship between the SVL of females and fecundity. Note this graph is shown only for illustrative purposes and was created with ordinary least squares linear model

3.2. Reproductive modes, fecundity, and SDI

The results of PGLS analysis were not significant (r 2 = .003, F 3,57 = 0.071, p = .98). There were no significant differences in the SDI of oviparous and viviparous lizards (β = 0.01 ± 0.05, t = 0.433, p = .67). Similarly, there were no significant effects of fecundity residuals on SDI (β = −0.005 ± 0.08, t = −0.063, p = .95). The model showed a high λ value (λ = 0.95), indicating a strong phylogenetic effect on the relationships between fecundity residuals and SSD.

3.3. Rensch's rule and ancestral reconstruction of SDI

The results of the major axis regression of independent contrasts indicated strong coevolution between females and males (r = .80; df = 58, p = .0001, Figure 2). The regression showed a slope significantly steeper than 1.0 (β = 1.17, r w = .29, p = .02; Figure 2). Most of the taxa (46 species, 75%) showed male‐biased SSD, and 14 species (23%) showed some degree of female‐biased SSD. The males and females of only one species showed similar body sizes (S. edwardtaylori). The SDI reconstruction showed six independent origins of the female‐biased SSD. In a clade with male‐biased SSD (formosus group), the branch of S. cryptus and S. subpictus showed a female‐biased SSD. Other independent origin of female‐biased SSD was found in the scalaris (S. bicanthalis and S. scalaris) group. Another origin for undulatus group (S. olivaceus, S. occidentalis, S. virgatus, S. woodi, S. undulatus, S. consobrinus, and S. tristichus). Finally, three additional species independently evolved female‐biased SSD: S. utiformis (utiformis group), S. graciosus (gracious group), and S. melanorhinus (clarkii group; Figure 3).

Figure 2.

Figure 2

Open in a new tab

Independent contrasts of SVL of males as a function of SVL of females. The solid line indicates isometry (β = 1), while the dashed line denotes the allometric relationship between both variables as fitted by major axis regression. Values in parentheses indicate the upper and lower confidence interval (95%) for the slope and p value the probability for a β > 1

4. Discussion

Once we control for phylogenetic effects, our results confirm a strong relationship between female body size and fecundity, suggesting that in Sceloporus lizards selection on fecundity has had a main role on the evolution of female body size. However, regardless of the reproductive mode (oviparous or viviparous), the size of females of Sceloporus is similar and has evolved in a similar fashion. We must point out that the similar response in the relationship of body size with increase in the clutch/litter size between both reproductive modes does not imply that the overall reproductive output (i.e., reproductive fitness of the female's life) is similar. The potential impact of fecundity selection on the different reproductive modes may be underestimated (Niewiarowski et al., 2004; Pincheira‐Donoso & Hunt, 2015; Shine, 2005). Oviparous species like S. gadoviae, S. siniferus, S. undulatus, and S. variabilis may have multiple clutches in a reproductive season (i.e., per year; Cruz‐Elizalde & Ramírez‐Bautista, 2016; Ramirez‐Bautista et al., 2005; Ramírez‐Bautista et al., 2015; Vinegar, 1975b), whereas other species like S. magister, S. melanorhinus, and S. spinosus have just one clutch per year, but they may have more than one reproductive event in their life (Méndez‐de la Cruz et al., 2013; Parker & Pianka, 1973; Ramirez‐Bautista et al., 2006; Valdéz‐González & Ramírez‐Bautista, 2002). On the other hand, all viviparous species have one litter per year, but in the majority of species, females can have several reproductive events (Méndez–de la Cruz et al., 1998; Ramírez‐Bautista et al., 2014; Villagrán‐Santa Cruz, Hernández‐Gallegos, & Méndez‐de La Cruz, 2009).

The differences in the gestation period between reproductive modes do not have any impact on the evolution of SSD, but according to the Renchs' rule, the slope of the regression of males on females is significantly steeper, providing evidence of greater evolutionary divergence in male size than in female size. Fitch (1978) noted that the high variation of SSD in Sceloporus lizards, and the implications of sexual and natural selection in order to explain the differences in body size between females and males. For lizard species in which body size often determines male mating success, males are typically larger than females (Cox et al., 2007). Body size often determines success in agonistic encounters, and it is correlated with dominance and territoriality (Carpenter, 1995; Martins, 1994; McMann, 1993; Molina‐Borja et al., 1998; Perry et al., 2004). However, in other species, females are larger than males, suggesting that fecundity selection may have favored the evolution of larger‐than‐average female body size (Cox et al., 2003; Zamudio, 1998). Furthermore, as Sceloporus lizards follow Rensch's rule, it can be argued that this allometric trend is the result of sexual selection favoring large male body size and that the relative impact of sexual selection on males has been stronger than fecundity selection on female body size (Fairbairn, 1997; Fairbairn et al., 2007; Pincheira‐Donoso & Tregenza, 2011).

The reconstruction of the evolution of SSD in Sceloporus lizards suggests that the ancestor and most of the extant species show a pattern of male‐biased SSD. This could indicate that directional sexual selection acting on males has been greater than the selection acting on female fecundity. Territoriality and aggressive behaviors are common in Sceloporus: These are mainly associated with defense of mates in males (Martins, 1994), and resources (e.g., food, water, perches) in both sexes (Cooper & Wilson, 2007; Martins, 1994; Vinegar, 1975c; Woodley & Moore, 1999). In general, larger individuals have an advantage when defending territories in agonistic encounters (Martins, 1994; Swierk, 2014). However, female‐biased SSD has evolved independently at least six times (Figure 3). Perhaps in these taxa, selection on fecundity has been stronger than sexual selection. Nonetheless, it is possible that in these species, sexual selection has also favored small male body size (see Cox et al., 2007; Olsson et al., 2002), albeit there is no clear pattern as to the ecological factors associated with the evolution of female‐biased SSD. These species, like other Sceloporus species that show male‐biased SSD, live in different environments, including tropical deciduous forest, grasslands, scrubland, woodlands, and open coniferous forests, and can be found from sea level up to elevations >4,000 m. Moreover, species showing female‐biased SSD are oviparous and viviparous (e.g., undulatus group versus S. bicanthalis, respectively), and with single or multiples clutches per reproductive season (e.g., S. melanorhinus versus S. consobrinus, respectively). The diversity of ecological and social factors provides opportunities for changes in the direction and magnitude of natural and sexual selection between and within species. However, the information available for female preference and agonistic interactions between males are, in the majority of species, severely scarce or absent (see Martins, 1994; Swierk, 2014).

Previous studies in Phrynosomatidae do not support Rensch′s rule (Cox et al., 2007). However, these results could be obscured by the large diversity in morphology, behavior, ecology, and life‐history traits between different lizards genera (Cox et al., 2003). In addition, these studies do not consider the phylogenetic relationship between the species (see Cox et al., 2007). Conversely, our results are similar to previous studies in the genus Liolaemus (Liolaemidae). The clutch/litter size increases as a function of female body size. Nonetheless, fecundity is not correlated with SSD, but Lioalemus species appear to follow Rensch's rule (Pincheira‐Donoso & Tregenza, 2011). Both Sceloporus and Liolaemus species occupy a great diversity of environments, along wide latitudinal and altitudinal ranges and showing great variation in morphological, ecological, behavior, and life‐history traits (Pincheira‐Donoso, Scolaro, & Sura, 2008; Sites et al., 1992). The similarity between our results and those reported in Liolaemus suggests that fecundity selection may have driven the divergence in female body size but that the diversifying effects of sexual selection may often exceed fecundity selection on females in both genera.

The genus Sceloporus includes more than 90 species and has been proposed as a group with an accelerated diversification rate (Bell, Smith, & Chiszar, 2003; Leaché, 2010; Wiens et al., 2010). Sceloporus lizards have colonized diverse niches throughout its distribution range, from northern Panama to southwestern Canada, and show one of the widest altitudinal ranges for reptiles. Due to the broad spread of niches, it is likely that the relative impact of natural and sexual selection has changed along novel environmental conditions, generating divergence from the optimum body size of females and males. In any case, the causal mechanisms associated with changes in the direction of SSD bias toward females in this group remain an open question that demand further investigation.

Conflict of Interest

None declared.

Supporting information

 

Click here for additional data file. (259.2KB, docx)

Acknowledgments

This work was supported by CONACyT: Ciencia Básica grant No. 235987 to RCC. Víctor Hugo Jiménez Arcos acknowledges to Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México (UNAM), and CONACyT for doctoral scholarship (No. 377215). This article is a requirement for obtaining the degree of Doctor en Ciencias del Posgrado en Ciencias Biológicas, UNAM. The authors wish to thank Alejandro Serrano Meneses for his invaluable suggestions to improve an earlier version of the manuscript and to Christopher Blair for his invaluable suggestions to improve the English and overall manuscript quality. We thank R. Santos‐Bibiano for providing data from Sceloporus adleri, as well as C. M. Gómez‐Hurtado, A. H. Díaz de la Vega‐Pérez, A. Calzada‐Arciniega, M. Pérez‐Quintero, C. Toscano‐Flores, and M. Illescas‐Aparicio for their help in the field. We thank four anonymous reviewers who also made invaluable suggestions to the manuscript.

Jiménez‐Arcos, V. H. , Sanabria‐Urbán, S. and Cueva del Castillo, R. (2016), The interplay between natural and sexual selection in the evolution of sexual size dimorphism in Sceloporus lizards (Squamata: Phrynosomatidae). Ecology and Evolution, 7: 905–917. doi: 10.1002/ece3.2572

References

  1. Abell, A. J. (1999). Variation in clutch size and offspring size relative to environmental conditions in the lizard Sceloporus virgatus . Journal of Herpetology, 33(2), 173–180. [Google Scholar]
  2. Andersson, M. (1994). Sexual selection. Princeton: Princeton University Press. [Google Scholar]
  3. Ballinger, R. E. (1973). Comparative demography of two viviparous iguanid lizards (Sceloporus jarrovi and Sceloporus poinsetti). Ecology, 54(2), 269–283. [Google Scholar]
  4. Bastiaans, E. , Bastiaans, M. J. , Morinaga, G. , Gaytán, J. G. C. , Marshazrll, J. C. , Bane, B. , … Sinervo, B. (2014). Female preference for sympatric vs. allopatric male throat color morphs in the mesquite lizard (Sceloporus grammicus) species complex. PLoS One, 9(4), 44–48. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bell, E. L. , Smith, H. M. , & Chiszar, D. C. (2003). An annotated list of the species‐group names applied to the lizard genus Sceloporus . Acta Zoologica Mexicana, 174, 103–174. [Google Scholar]
  6. Benabid, M. (1994). Reproduction and lipid utilization of tropical populations of Sceloporus variabilis . Herpetologica Monographs, 8(1994), 160–180. [Google Scholar]
  7. Blair, F. W. (1960). The rusty lizard, a population study. Austin: University of Texas Press. [Google Scholar]
  8. Blanckenhorn, W. U. (2000). The evolution of body size: What keeps organism small?. 75(4), 385–407. [DOI] [PubMed] [Google Scholar]
  9. Blanckenhorn, W. U. W. (2005). Behavioral causes and consequences of sexual size dimorphism. Ethology, 111(11), 977–1016. [Google Scholar]
  10. Braña, F. (1996). Sexual dimorphism in lacertid lizards: Male head increase vs female abdomen increase? Oikos, 75(3), 511–523. [Google Scholar]
  11. Burkholder, G. L. , & Tanner, W. W. (1974). Life history ecology of the Great Basin sagebrush swift, Sceloporus graciosus graciosus Baird and Girard, 1853. Brigham Young University Science Bulletin. Biological Series, 14(5), 1–42. [Google Scholar]
  12. Bustos‐Zagal, M. G. , Méndez‐de la Cruz, F. R. , Castro‐Franco, R. , & Villagrán‐Santa Cruz, M. (2011). Ciclo reproductor de Sceloporus ochoterenae en el estado de Morelos, México. Revista Mexicana de Biodiversidad, 82, 589–597. [Google Scholar]
  13. Butler, M. A. , & Losos, J. B. (2002). Multivariate sexual dimorphism, sexual selection, and adaptation in greater antillean Anolis lizards. Ecological Monographs, 72(4), 541–559. [Google Scholar]
  14. Butler, M. , Schoener, T. W. , & Losos, J. B. (2000). The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards. Evolution, 54(1), 259–272. [PubMed] [Google Scholar]
  15. Calder, W. A. (1984). Size, function and life history, Cambridge, MA: Harvard University Press. [Google Scholar]
  16. Calderón‐Espinosa, M. L. , Andrews, R. M. , & Méndez de la Cruz, F. R. (2006). Evolution of Egg retention in the Sceloporus spinosus group: Exploring the role of physiological, environmental, and phylogenetic factors. Herpetological Monographs, 20, 147. [Google Scholar]
  17. Calisi, R. M. , & Hews, D. K. (2007). Steroid correlates of multiple color traits in the spiny lizard, Sceloporus pyrocephalus . Journal of Comparative Physiology B, 177, 641–654. [DOI] [PubMed] [Google Scholar]
  18. Carbajal‐Márquez, R. A. , & Quintero‐Díaz, G. E. (2013). Natural history: Sceloporus scalaris clutch size. Herpetological Review, 44(4), 660–661. [Google Scholar]
  19. Carpenter, C. C. (1978). Comparative display behavior in the genus Sceloporus (Iguanidae). Contributions in Biology and Geology to the Milwaukee Public Museum, 18, 1–71. [Google Scholar]
  20. Carpenter, G. C. (1995). Modeling dominance: The influence of size, coloration, and experience on dominance relations in tree lizards (Urosaurus ornatus). Herpetologica Monographs, 9(1995), 88–101. [Google Scholar]
  21. Cooper, W. E. , & Wilson, D. S. (2007). Sex and social costs of escaping in the striped plateau lizard Sceloporus virgatus . Behavioral Ecology, 18(4), 764–768. [Google Scholar]
  22. Cox, R. M. , Butler, M. A. , & John‐Alder, H. B. (2007). The evolution of sexual size dimorphism in reptiles In Fairbairn D. J., Blanckenhorn W. U., & Székely T. (Eds.), Sex, size and gender roles: Evolutionary studies of sexual size dimorphism. Oxford, UK: Oxford University Press. [Google Scholar]
  23. Cox, R. M. , Skelly, S. L. , & John‐Alder, H. B. (2003). A comparative test of adaptive hypotheses for sexual size dimorphism in lizards. Evolution, 57(7), 1653–1669. [DOI] [PubMed] [Google Scholar]
  24. Cruz‐Elizalde, R. , & Ramírez‐Bautista, A. (2016). Reproductive cycles and reproductive strategies among populations of the Rose‐bellied Lizard Sceloporus variabilis (Squamata: Phrynosomatidae) from central Mexico. Ecology and Evolution, 6(6), 1753–1768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Dornhaus, A. , Powell, S. , & Bengston, S. (2012). Group size and its effects on collective organization. Annual Review of Entomology, 57(1), 123–141. [DOI] [PubMed] [Google Scholar]
  26. Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: Pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics, 28(1997), 659–687. [Google Scholar]
  28. Fairbairn, D. J. , Blanckenhorn, W. U. , & Székely, T. (2007). Sex, size & gender roles. Evolutionary studies of sexual size dimorphism. Oxford, UK: Oxford University Press. [Google Scholar]
  29. Felsenstein, J. (1985). Phylogenies and the comparative method. The American Naturalist, 125(1), 1–15. [Google Scholar]
  30. Feria Ortiz, M. , Salgado Ugarte, I. H. , & Nieto‐Montes de Oca, A. (2001). Diet and reproductive biology of the viviparous lizard Sceloporus torquatus torquatus (Squamata: Phrynosomatidae). Journal of Herpetology, 35(1), 104–112. [Google Scholar]
  31. Fitch, H. S. (1978). Sexual size differences in the genus Sceloporus . University of Kansas Science Bulletin the University of Kansas Science Bulletin, 51(13), 441–461. [Google Scholar]
  32. Fitch, H. S. (1985). Variation in clutch and litter size in new world reptiles. Miscellaneous Publications of the Museum of Natural History of the University of Kansas, 76, 1–76. [Google Scholar]
  33. Fitzgerald, L. A. , Painter, C. W. , Hibbits, T. J. , Ryberg, W. A. , & Smolensky, N. (2011). The Range and Distribution of Sceloporus arenicolus in Texas: Results of surveys conducted 8–15 June 2011, Texas. Retrieved from http://irnr.tamu.edu/media/285120/tx_dsl_final.pdf
  34. Foellmer, M. W. , & Moya‐Laraño, J. (2007). Sexual size dimorphism in spiders: Patterns and processes In Fairbairn D. J., Blanckenhorn W. U. & Székely T. (Eds.), Sex, size & gender roles. Evolutionary studies of sexual size dimorphism (pp. 38–49). Oxford, UK: Oxford University Press. [Google Scholar]
  35. Gadsden, H. , & Estrada‐Rodríguez, J. L. (2007). Ecology of the spiny lizard Sceloporus jarrovii in the Central Chihuahuan Desert. The Southwestern Naturalist, 52(4), 600–608. [Google Scholar]
  36. Gadsden, H. , Rodríguez‐Romero, F. D. J. , de Méndez‐ la Cruz, F. R. , & Gil‐Martínez, R. (2005). Ciclo reproductor de Sceloporus poinsettii Baird Y Girard 1852 (squamata: Phrynosomatidae) en el centro del Desierto Chihuahuense, México. Acta Zoologica Mexicana, 21(3), 93–107. [Google Scholar]
  37. Galina Tessaro, P. , Aguilera‐Miller, E. F. , & Álvarez‐Castañeda, S. T. (2015). Contribución a la distribución, ecología y estado de conservación de dos especies del género Sceloporus, endémicas de la región del Cabo, Baja California Sur, México, DF: Retrieved from http://www.conabio.gob.mx/institucion/proyectos/resultados/InfHK012.pdf [Google Scholar]
  38. García de la Peña, C. , Contreras‐Balderas, A. , Castañeda, G. , & Lazcano, D. (2004). Infestación y distribución corporal de la nigua Eutrombicula alfreddugesi (Acari: Trombiculidae) en el lacertilio de las rocas Sceloporus couchii (Sauria: Phrynosomatidae). Acta Zoológica Mexicana, 20(2), 159–165. [Google Scholar]
  39. García‐de la Peña, C. , Castañeda, G. , & Lazcano, D. (2005). Observations on Ectoparasitism by Eutrombicula alfreddugesi (Acari: Trombiculidae) in a population of Sceloporus cyanogenys . Bulletin of the Chicago Herpetological Society, 40(3), 52–53. [Google Scholar]
  40. García‐Vázquez, U. O. , Trujano‐Ortega, M. , & Contreras‐Arquieta, A. (2014). Natural history: Reproduction of Sceloporus parvus . Herpetological Review, 45(3), 507. [Google Scholar]
  41. Gibbons, J. W. (1992). A review of techniques for quantifying sexual size dimorphism. Growth, Development & Aging, 56(4), 269–281. [PubMed] [Google Scholar]
  42. Godinez‐Cano, E. (1985). Ciclo reproductivo de Sceloporus megalepidurus megalepidurus Smith (Reptilia: Sauria: Iguanidae), en la parte oriental de Tlaxcala, México, Bachelor thesis. Universidad Nacional Autónoma de México, México, DF. [Google Scholar]
  43. Goldberg, S. R. (2014). Natural history: Reproduction in Sceloporus angustus . Herpetological Review, 45(4), 699. [Google Scholar]
  44. Goldberg, S. R. , & Beaman, K. R. (2004). Reproduction in the san lucas banded rock lizard, Petrosaurus thalassinus (Phrynosomatidae) from Baja California Sur, Mexico. Bulletin of the Southern California Academy of Sciences, 103(3), 147–149. [Google Scholar]
  45. Gonzalez‐Voyer, A. , & Kolm, N. (2010). Sex, ecology and the brain: Evolutionary correlates of brain structure volumes in tanganyikan cichlids. PLoS One, 5(12), 1–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Grant, B. W. , & Dunham, A. E. (1990). Elevational covariation in environmental constraints and life histories of the desert lizard Sceloporus merriami . Ecology, 71(5), 1765–1776. [Google Scholar]
  47. Grummer, J. A. , Calderón‐Espinosa, M. L. , Nieto‐Montes de Oca, A. , Smith, E. N. , Méndez‐de la Cruz, F. R. , & Leaché, A. D. (2015). Estimating the temporal and spatial extent of gene flow among sympatric lizard populations (genus Sceloporus) in the southern Mexican highlands. Molecular Ecology, 24(7), 1523–1542. [DOI] [PubMed] [Google Scholar]
  48. Guillette, L. J. , & Méndez‐de la Cruz, F. R. (1993). The reproductive cycle of the viviparous Mexican lizard Sceloporus torquatus . Journal of Herpetology, 27(2), 168–174. [Google Scholar]
  49. Harvey, P. H. , & Pagel, M. D. (1991). The comparative method in evolutionary biology. Oxford, UK: Oxford Series in Ecology and Evolution. [Google Scholar]
  50. Hedrick, A. V. , & Temeles, E. J. (1989). The evolution of sexual dimorphism in animals: Hypotheses and tests. Trends in Ecology and Evolution, 4(5), 136–138. [DOI] [PubMed] [Google Scholar]
  51. Herrel, A. , Meyers, J. J. , & Vanhooydonck, B. (2002). Relations between microhabitat use and limb shape in phrynosomatid lizards. Biological Journal of the Linnean Society, 77(1), 149–163. [Google Scholar]
  52. Jackson, J. F. , & Telford, S. R. J. (1974). Reproductive ecology of the Florida scrub lizard Sceloporus woodi . Copeia, 1974(3), 689–694. [Google Scholar]
  53. Jiménez‐Arcos, V. H. (2013). Variación fenotípica asociada a la coloración sexual en una población de Sceloporus aeneus (Squamata: Phrynosomatidae), Master thesis. Universidad Nacional Autónoma de México, México, DF: 69 p. [Google Scholar]
  54. Jiménez‐Cruz, E. , Ramírez‐Bautista, A. , Marshall, J. C. , Lizana‐Avia, M. , & Nieto‐Montes de Oca, A. (2005). Reproductive cycle of Sceloporus grammicus (Squamata: Phrynosomatidae) From Teotihuacán, México. The Southwestern Naturalist, 50(2), 178–187. [Google Scholar]
  55. Köhler, G. , & Heimes, P. (2002). Stachelleguane. Germany: Herpeton, Verlag. [Google Scholar]
  56. Kumar, S. , Stecher, G. , & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, p.msw054. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/27004904 [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Lanfear, R. , Calcott, B. , Kainer, D. , Mayer, C. , & Stamatakis, A. (2014). Selecting optimal partitioning schemes for phylogenomic datasets. BMC evolutionary biology, 14(1), 1–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Leaché, A. D. (2010). Species trees for spiny lizards (Genus Sceloporus): Identifying points of concordance and conflict between nuclear and mitochondrial data. Molecular Phylogenetics and Evolution, 54(1), 162–171. [DOI] [PubMed] [Google Scholar]
  59. Leaché, A. D. , Banbury, B. L. , Linkem, C. W. , & de Oca, A. N. M. (2016). Phylogenomics of a rapid radiation: Is chromosomal evolution linked to increased diversification in North American spiny lizards (Genus Sceloporus)? BMC evolutionary biology, 16(1), 63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Lemos‐Espinal, J. A. , & Dixon, J. R. (2013). Amphibians and reptiles of San Luis Potosí. Eagle Mountain: Eagle Mountain Publishing. [Google Scholar]
  61. Lemos‐Espinal, J. A. , & Smith, H. M. (2007). Anfibios y Reptiles del Estado de Chihuahua, México/Amphibians and reptiles of the State of Chihuahua, México. México, DF: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. [Google Scholar]
  62. Lemos‐Espinal, J. A. , Smith, G. R. , & Ballinger, R. E. (1999). Reproduction in Gadow's spiny lizard, Sceloporus gadoviae (Phrynosomatidae), from arid tropical México. The Southwestern Naturalist, 44(1), 57–63. [Google Scholar]
  63. Losos, J. B. (1990). The evolution of form and function: Morphology and Locomotor performance in West Indian Anolis lizards. Evolution, 44(5), 1189–1203. [DOI] [PubMed] [Google Scholar]
  64. Maddison, W. P. (1997). Gene trees in species trees. Systematic Biology, 46(3), 523–536. [Google Scholar]
  65. Maddison, W. P. , & Maddison, D. R. (2015). Mesquite: A modular system for evolutionary analysis Version 3.04. Retrieved from http://mesquiteproject.org
  66. Martin, R. F. (1973). Reproduction in the tree lizard (Urosaurus ornatus) in central Texas; drought conditions. Herpetologica, 29(1), 27–32. [Google Scholar]
  67. Martínez Bernal, R. L. (2004). Contribución al conocimiento de la biología de la especie endémica Sceloporus macdougalli en el Istma de Tehuantepec, Oaxaca, México, Bachelor thesis. Universidad Nacional Autónoma de México, México, DF. [Google Scholar]
  68. Martins, E. P. (1994). Phylogenetic perspectives on the Evolution of lizard territoriality In Vitt L. J. & Pianka E. R. (Eds.), Lizard ecology: Historical and experimental perspectives (pp. 117–144). Princeton: Princeton University Press. [Google Scholar]
  69. Martins, E. P. , & Hansen, T. F. (1997). Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into the analysis of interspecific data. The American Naturalist, 149(4), 646–667. [Google Scholar]
  70. Mayhew, W. W. (1963). Reproduction in the granite spiny lizard, Sceloporus orcutti . Copeia, 1963(1), 144–152. [Google Scholar]
  71. McMann, S. (1993). Contextual signalling and the structure of dyadic encounters in Anolis carolinensis . Animal Behaviour, 46, 657–668. [Google Scholar]
  72. Méndez–de la Cruz, F. R. , Villagrán‐Santa Cruz, M. , & Andrews, R. M. (1998). Evolution of viviparity in the lizard genus Sceloporus . Herpetologica, 54(4), 521–532. [Google Scholar]
  73. Méndez‐De La Cruz, F. R. , Villagrán‐Santa Cruz, M. , López‐Ortíz, M. L. , & Hernández‐Gallegos, O. (2013). Reproductive cycle of a high‐elevation, oviparous lizard (Sceloporus spinosus: Reptilia: Phrynosomatidae). The Southwestern Naturalist, 58(1), 54–63. [Google Scholar]
  74. Molina‐Borja, M. , Padron‐Fumero, M. , & Alfonso‐Martin, T. (1998). Morphological and behavioural traits affecting the intensity and outcome of male contests in Gallotia galloti galloti (Family Lacertidae). Ethology, 104(4), 314–322. [Google Scholar]
  75. Niewiarowski, P. H. , Angilletta Jr, M. J. , & Leaché, A. D. (2004). Phylogenetic comparative analysis of life‐history variation among populations of the lizard Sceloporus undulatus: An example and prognosis. Evolution, 58(3), 619–633. [DOI] [PubMed] [Google Scholar]
  76. Olsson, M. , Shine, R. , Wapstra, E. , Ujvari, B. , & Madsen, T. (2002). Sexual dimorphism in lizard body shape: The roles of sexual selection and fecundity selection. Evolution, 56(7), 1538–1542. [DOI] [PubMed] [Google Scholar]
  77. Orme, D. , Freckleton, R. , Thomas, G. , Petzoldt, T. , Fritz, S. , Isaac, N. , & Pearse, W. (2012). Caper: Comparative Analyses of Phylogenetics and Evolution in R. Version 0.5. Retrieved from http://cran.r-project.org/web/packages/caper/caper.pdf
  78. Ortega‐León, A. M. , Smith, E. R. , Zúñiga‐Vega, J. J. , & Méndez‐de la Cruz, F. R. (2007). Growth and demography of one population of the Lizard Sceloporus mucronatus mucronatus . Western North American Naturalist, 67(4), 492–502. [Google Scholar]
  79. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877–884. [DOI] [PubMed] [Google Scholar]
  80. Paradis, E. , Claude, J. , & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20(2), 289–290. [DOI] [PubMed] [Google Scholar]
  81. Parker, W. S. , & Pianka, E. R. (1973). Notes on the ecology of the iguanid lizard. Sceloporus Magister, 29(2), 143–152. [Google Scholar]
  82. Pérez‐Ramos, E. , & Saldaña de La Riva, L. (2008). Morphological revision of lizards of the formosus group, genus Sceloporus (Squamata: Sauria) of southern México, with description of a new species. Bulletin of the Maryland Herpetological Society, 44(3), 77–97. [Google Scholar]
  83. Perry, G. , LeVering, K. , Girard, I. , & Garland, T. (2004). Locomotor performance and social dominance in male Anolis cristatellus . Animal Behaviour, 67(1), 37–47. [Google Scholar]
  84. Pincheira‐Donoso, D. , & Hunt, J. (2015). Fecundity selection theory: Concepts and evidence. Biological Reviews, 2015, 1–16. [DOI] [PubMed] [Google Scholar]
  85. Pincheira‐Donoso, D. , Scolaro, A. J. , & Sura, P. (2008). A monographic catalogue on the systematics and phylogeny of the South American iguanian family Liolaemidae (Squamata, Iguania). Zootaxa, 1800(2008), 1–85. [Google Scholar]
  86. Pincheira‐Donoso, D. , & Tregenza, T. (2011). Fecundity selection and the evolution of reproductive output and sex‐specific body size in the Liolaemus lizard adaptive radiation. Evolutionary Biology, 38(2), 197–207. [Google Scholar]
  87. Qualls, C. P. , & Shine, R. (1995). Maternal body‐volume as a constraint on reproductive output in lizards: Evidence from the evolution of viviparity. Oecologia, 103(1995), 73–78. [DOI] [PubMed] [Google Scholar]
  88. Rambaut, A. , & Drummond, A. (2013). Tracer V1.6 [Internet]. Retrieved from http://beast.bio.ed.ac.uk/software/
  89. Ramírez‐Bautista, A. , & Dávila‐Ulloa, E. (2009). Reproductive characteristics of a population of Sceloporus dugesii (Squamata: Phrynosomatidae) from Michoacán, Mexico. The Southwestern Naturalist, 54(4), 400–408. [Google Scholar]
  90. Ramírez‐Bautista, A. , & Gutiérrez‐Mayén, G. (2003). Reproductive ecology of Sceloporus utiformis (Sauria: Phrynosomatidae) from a Tropical Dry Forest of México. Journal of Herpetology, 37(1), 1–10. [Google Scholar]
  91. Ramírez‐Bautista, A. , & Olvera Becerril, V. (2004). Reproduction in the boulder spiny lizard, Sceloporus pyrocephalus (Sauria : Phrynosomatidae), from a Tropical Dry Forest of México. Journal of Herpetology, 38(2), 225–231. [Google Scholar]
  92. Ramírez‐Bautista, A. , & Pavón, N. P. (2009). Sexual dimorphism and reproductive cycle in the arboreal spiny lizard Sceloporus formosus Wiegmann (Squamata: Phrynosomatidae) from central Oaxaca, Mexico. Revista Chilena de Historia Natural, 82(4), 553–563. [Google Scholar]
  93. Ramírez‐Bautista, A. , Stephenson, B. P. , Hernández‐Íbarra, X. , Hernández‐Salinas, U. , Cruz‐Elizalde, R. , Lozano, A. , & Smith, G. R. (2012). Reproductive strategy of male and female eastern Sceloporus spinosus (Squamata, Phrynosomatidae), México. Acta Herpetologica, 7(2), 239–252. [Google Scholar]
  94. Ramírez‐Bautista, A. , Stephenson, B. P. , Lozano, A. , Uribe‐Rodríguez, H. , & Leyte Manrique, A. (2012). Atypical reproductive cycles in a population of Sceloporus grammicus (Squamata: Phrynosomatidae) from the Mexican Plateau. Ecology and Evolution, 2(8), 1903–1913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Ramírez‐Bautista, A. , Uribe‐Peña, Z. , & Guillette, L. J. J. (1995). Reproductive biology of the lizard Urosaurus bicarinatus bicarinatus (Reptilia: Phrynosomatidae) from Rio Balsas Basin, Mexico. Herpetologica, 51(1), 24–33. [Google Scholar]
  96. Ramirez‐Bautista, A. , & Vitt, L. J. (1998). Reproductive biology of Urosaurus bicarinatus (Sauria: Phrynosomatidae) from a tropical dry forest of Mexico. The Southwestern Naturalist, 43(3), 381–390. [Google Scholar]
  97. Ramirez‐Bautista, A. , Ortíz‐Cruz, A. L. , Del Coro Arizmendi, M. , & Campos, J. (2005). Reproductive characteristics of two syntopic lizard species, Sceloporus gadoviae and Sceloporus jalapae (Squamata: Phrynosomatidae), from Tehuacan Valley, Puebla, Mexico. Western North American Naturalist, 65(2), 202–209. [Google Scholar]
  98. Ramirez‐Bautista, A. , Balderas‐Valdivia, C. , & Ortiz‐Pulido, R. (2006). Reproductive cycle of male and female spiny lizards, Sceloporus melanorhinus, in a tropical dry forest. The Southwestern Naturalist, 51(2), 157–162. [Google Scholar]
  99. Ramírez‐Bautista, A. , Ramos‐Flores, O. , Stephenson, B. P. , & Smith, G. R. (2008). Reproduction and sexual dimorphism in two populations of Sceloporus minor of the Guadalcázar Region, San Luis Potosí, Mexico. Herpetological Journal, 18, 121–127. [Google Scholar]
  100. Ramírez‐Bautista, A. , Stephenson, B. P. , Serrano Muñoz, C. , Cruz‐Elizalde, R. , & Hernández‐Salinas, U. (2014). Reproduction and sexual dimorphism in two populations of the polymorphic spiny lizard Sceloporus minor from Hidalgo, México. Acta Zoologica, 95(4), 397–408. [Google Scholar]
  101. Ramírez‐Bautista, A. , Luría‐Manzano, R. , Cruz‐Elizalde, R. , Pavón, N. P. , & David Wilson, L. (2015). Variation in reproduction and sexual dimorphism in the long‐tailed spiny lizard, Scelopors siniferus, from the southern Pacific coast of Mexico. Salamandra, 51(2), 73–82. [Google Scholar]
  102. Ramírez‐Pinilla, M. P. , Calderón‐Espinosa, M. L. , Flores‐Villela, O. , Muñoz‐Alonso, A. , & de la Cruz, F. R. M. (2009). Reproductive activity of three sympatric viviparous lizards at omiltemi, Guerrero, Sierra Madre del Sur, Mexico. Journal of Herpetology, 43(3), 409–420. [Google Scholar]
  103. Reiss, M. J. (1989). The allometry of growth and reproduction. Cambridge: Cambridge University Press. [Google Scholar]
  104. Rensch, B. (1950). Die Abhängigkeit der relativen Sexual differenzvon der Körpergrösse. Bonner Zoologische Beiträge, 1, 58–69. [Google Scholar]
  105. Revell, L. J. (2010). Phylogenetic signal and linear regression on species data. Methods in Ecology and Evolution, 1(4), 319–329. [Google Scholar]
  106. Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2), 217–223. [Google Scholar]
  107. Revell, L. J. (2013). Two new graphical methods for mapping trait evolution on phylogenies. Methods in Ecology and Evolution, 4(8), 754–759. [Google Scholar]
  108. Revell, L. J. (2014). Modern phylogenetic comparative methods and their application in evolutionary biology. Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology, 77–103. Retrieved from http://link.springer.com/10.1007/978-3-662-43550-2 [Google Scholar]
  109. Rodríguez‐Romero, F. J. , Méndez de la, C. F. R. , Hernández, G.O. , & Velázquez, R. (2010). Fenología reproductora de alta montaña en dos especies de lacertilios emparentados (Squamata: Phrynosomatidae) In Hernández‐Gallegos O., de Méndez– la Cruz F. R., & Méndez‐Sánches F. J. (Eds.), Reproducción en reptiles: Morfología, ecología y evolución (p. 169). Toluca: Universidad Autónoma del Estado de México. [Google Scholar]
  110. Romero‐Schmidt, H. L. , Ortega‐Rubio, A. , & Acevedo‐Beltran, M. (1999). Reprodudive charaderistics of the black‐tailed brush lizard, Urosaurus nigricaudus (Phrynosomatidae). Revista de Biologia Tropical, 47(4), 1111–1115. [Google Scholar]
  111. Ronquist, F. , Teslenko, M. , van der Mark, P. , Ayres, D. L. , Darling, A. , Höhna, S. , … Huelsenbeck, J. P. (2012). Mrbayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Ruckstuhl, K. E. , & Neuhaus, P. (2005). Sexual Segregation in Vertebrates. Ecology of the Two Sexes. Cambridge: Cambridge University Press. [Google Scholar]
  113. Sanabria‐Urbán, S. , Song, H. , Oyama, K. , González‐Rodríguez, A. , Serrano‐Meneses, M. A. , & Cueva del Castillo, R. (2015). Body size adaptations to altitudinal climatic variation in neotropical grasshoppers of the genus Sphenarium (Orthoptera: Pyrgomorphidae). PLoS One, 10(12), e0145248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  114. Sanderson, M. J. (2002). Estimating absolute rates of molecular evolution and divergence times: A penalized likelihood approach. Molecular Biology and Evolution, 19(1), 101–109. [DOI] [PubMed] [Google Scholar]
  115. Scharf, I. , & Meiri, S. (2013). Sexual dimorphism of heads and abdomens: Different approaches to “being large”in female and male lizards. Biological Journal of the Linnean Society, 665–673. [Google Scholar]
  116. Shine, R. (1989). Ecological causes for the evolution of sexual dimorphism: A review of the evidence. The Quarterly Review of Biology, 64(4), 419–461. [DOI] [PubMed] [Google Scholar]
  117. Shine, R. (2005). Life‐history evolution in reptiles. Annual Review of Ecology, Evolution, and Systematics, 36(1), 23–46. [Google Scholar]
  118. Sites, J. W. , Archie, J. W. , Cole, C. J. , & Flores‐Villela, O. (1992). A review of phylogenetic hypotheses for lizards of the genus Sceloporus (Phrynosomatidae): Implications for ecological and evolutionary studies. Bulletin of the American Museum of Natural History, 213, 1–110. A1992HZ58300001. [Google Scholar]
  119. Smith, H. M. (1939). The Mexican and Central American lizards of the genus Sceloporus . Field Museum of Natural History. Zoological Series, 26(1), 1–397. [Google Scholar]
  120. Smith, G. , & Lemos‐Espinal, J. (2003). Body size, sexual dimorphism, and clutch size in two populations of the lizard Sceloporus ochoteranae . Southwestern Naturalist, 48(1), 123–126. [Google Scholar]
  121. Stephenson, B. P. , & Ramírez‐Bautista, A. (2012). Did sexually dimorphic dorsal coloration evolve by a pre‐existing bias in males in the lizard Sceloporus minor? Evolutionary Ecology, 26(5), 1277–1291. [Google Scholar]
  122. Stillwell, R. , Blanckenhorn, W. U. , Teder, T. , Davidowitz, G. , & Fox, C. W. (2010). Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: From physiology to evolution. Annual Review of Entomology, 55, 227–245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  123. Stuart‐Fox, D. (2009). A test of Rensch's rule in dwarf chameleons (Bradypodion spp.), a group with female‐biased sexual size dimorphism. Evolutionary Ecology, 23(3), 425–433. [Google Scholar]
  124. Swierk, L. N. (2014). Mate choice and competition in the eastern fence lizard, Sceloporus undulatus. PhD dissertation: The Pennsylvania State University. [Google Scholar]
  125. Tinkle, D. W. (1973). A population analysis of the sagebrush lizard, Sceloporus graciosus in Southern Utah. Copeia, 1973(2), 284–296. [Google Scholar]
  126. Valdéz‐González, M. A. , & Ramírez‐Bautista, A. (2002). Reproductive characteristics of the spiny lizards, Sceloporus horridus and Sceloporus spinosus (Squamata: Phrynosomatidae) from México. Journal of Herpetology, 36(1), 36–43. [Google Scholar]
  127. Van Loben Sels, R. C. , & Vitt, L. J. (1984). Desert lizard reproduction: Seasonal and annual variation in Urosaurus ornatus (Iguanidae). Canadian Journal of Zoology, 62, 1779–1787. [Google Scholar]
  128. Villagrán‐Santa Cruz, M. , Hernández‐Gallegos, O. , & Méndez‐de La Cruz, F. R. (2009). Reproductive cycle of the lizard Sceloporus mucronatus with comments on intraspecific geographic variation. Western North American Naturalist, 69(4), 437–446. [Google Scholar]
  129. Vinegar, M. A. (1975a). Comparative aggression in Sceloporus virgatus, S. undulatus consobrinus, and S. u. tristichus (Sauria: Iguanidae). Animal Behaviour, 23(PART 2), 279–286. [DOI] [PubMed] [Google Scholar]
  130. Vinegar, M. B. (1975b). Demography of the striped plateau lizard, Sceloporus virgatus . Ecological Society of America, 56(1), 172–182. [Google Scholar]
  131. Vinegar, M. B. (1975c). Life history phenomena in two populations of the lizard Sceloporus undulatus in southwestern New Mexico. American Midland Naturalist, 93(2), 388–402. [Google Scholar]
  132. Vitt, L. J. (1977). Observations on clutch and egg size and evidence for multiple clutches in some lizards of southwestern United States. Herpetologica, 33(3), 333–338. [Google Scholar]
  133. Vitt, L. J. , Van Loben Sels, R. C. , & Ohmart, R. D. (1978). Lizard reproduction: Annual variation and environmental correlates in the iguanid lizard Urosaurus graciosus . Herpetologica, 34(3), 241–253. [Google Scholar]
  134. Warton, D. I. , Wright, I. J. , Falster, D. S. , & Westoby, M. (2006). Bivariate line‐fitting methods for allometry. Biological Reviews, 81(2), 259–291. [DOI] [PubMed] [Google Scholar]
  135. Warton, D. I. , Duursma, R. A. , Falster, D. S. , & Taskinen, S. (2012). Smatr 3‐ an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution, 3(2), 257–259. [Google Scholar]
  136. Webb, T. J. , & Freckleton, R. P. (2007). Only half right: Species with female‐biased Sexual Size Dimorphism consistently break Rensch's rule. PLoS One, 2(9). [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Weiss, S. L. (2006). Female‐specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behavioral Ecology, 17, 726–732. [Google Scholar]
  138. Wiens, J. J. , Kozak, K. H. , & Silva, N. (2013). Diversity and niche evolution along aridity gradients in north american lizards (Phrynosomatidae). Evolution, 67(6), 1715–1728. [DOI] [PubMed] [Google Scholar]
  139. Wiens, J. J. , & Reeder, T. W. (1997). Phylogeny of the spiny lizards (Sceloporus) based on molecular and morphological evidence. Herpetological Monographs, 11(1997), 1–101. [Google Scholar]
  140. Wiens, J. J. , Reeder, T. W. , & Nieto Montes de Oca, A. (1999). Molecular phylogenetics and evolution of sexual dichromatism among populations of the yarrow's spiny lizard (Sceloporus jarrovi). Evolution, 53(6), 1884–1897. [DOI] [PubMed] [Google Scholar]
  141. Wiens, J. J. , Kuczynski, C. A. , Arif, S. , & Reeder, T. W. (2010). Phylogenetic relationships of phrynosomatid lizards based on nuclear and mitochondrial data, and a revised phylogeny for Sceloporus . Molecular Phylogenetics and Evolution, 54(1), 150–161. [DOI] [PubMed] [Google Scholar]
  142. Williams, S. C. (2010). Sources and Consequences of Ecological Intraspecific Variation in the Florida Scrub Lizard (Sceloporus woodi). Georgia Southern University; Electronic Theses & Dissertations. Retrieved from http://digitalcommons.georgiasouthern.edu/etd Recommended. [Google Scholar]
  143. Woodley, S. , & Moore, M. (1999). Female territorial aggression and steroid hormones in mountain spiny lizards. Animal Behaviour, 57(5), 1083–1089. [DOI] [PubMed] [Google Scholar]
  144. Yan‐Yan, S. , Du, Y. , Yang, J. , Fu, T. B. , Lin, C. X. , & Ji, X. (2012). Is the evolution of viviparity accompanied by a relative increase in maternal abdomen size in lizards? Evolutionary Biology, 39(3), 388–399. [Google Scholar]
  145. Zamudio, K. R. (1998). The evolution of female‐biased sexual size dimorphism: A population‐level comparative study in horned lizards (Phrynosoma). Evolution, 52(6), 1821–1833. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

 

Click here for additional data file. (259.2KB, docx)

Articles from Ecology and Evolution are provided here courtesy of Wiley

RESOURCES